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Marine sponge microbial association: Towards disclosing unique symbiotic interactions
Accepted Manuscript Marine sponge microbial association: Towards disclosing unique symbiotic interactions G. Seghal Kiran, Sivasankari Sekar, Pasiyappazham Ramasamy, Thangadurai Thinesh, Saqib Hassan, Anuj Nishanth Lipton, A.S. Ninawe, Joseph Selvin PII:
S0141-1136(17)30668-2
DOI:
10.1016/j.marenvres.2018.04.017
Reference:
MERE 4513
To appear in:
Marine Environmental Research
Received Date: 2 November 2017 Revised Date:
1 March 2018
Accepted Date: 25 April 2018
Please cite this article as: Kiran, G.S., Sekar, S., Ramasamy, P., Thinesh, T., Hassan, S., Lipton, A.N., Ninawe, A.S., Selvin, J., Marine sponge microbial association: Towards disclosing unique symbiotic interactions, Marine Environmental Research (2018), doi: 10.1016/j.marenvres.2018.04.017. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Marine sponge microbial association: towards disclosing unique symbiotic interactions
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G. Seghal Kirana, Sivasankari Sekarb, Pasiyappazham Ramasamyb, Thangadurai Thineshc, Saqib Hassanb, Anuj Nishanth Liptonb, A.S. Ninawed, Joseph Selvinb*
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b
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c
Florida International University, Miami, Florida - 33199
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d
Department of Biotechnology, Ministry of Science and Technology, New Delhi, India
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*Corresponding author (J. Selvin):
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Department of Microbiology, School of Life Sciences, Pondicherry University, Puducherry –
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605014, India. Email: [email protected], [email protected]
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Department of Food Science and Technology, Pondicherry University, Puducherry – 605014, India.
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Department of Microbiology, School of Life Sciences, Pondicherry University, Puducherry – 605014, India
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1. Introduction
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2. Insights of sponge-eukaryotic symbionts
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2.1. Sponge-algae symbiosis
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2.2. Sponge- fungi symbiosis
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2.3. Sponge- yeast symbiosis
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2.4. Sponge- polychaetes symbiosis
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2.5. Sponge- barnacles symbiosis
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2.6. Sponge- mangroves symbiosis
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2.7. Sponge- other symbiosis 3. Sponge-specific microbial symbionts
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3.1. Functional ecology of symbiosis
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3.2. Sponge- bacterial symbiosis
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3.3. Sponge- Actinobacteria symbiosis
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3.4. Sponge- Cyanobacteria symbiosis
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4. Nutritional association of sponges and its holobionts
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4.1. Sponge- holobiont symbiosis
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4.2. Nitrogen metabolism
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4.3. Carbon fixation
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4.4. Other metabolism
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5. Dynamics of sponge microbiome
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5.1. Environmental factors
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6. Sponge-coral association: invasive or beneficial?
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6.1. Beneficial
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6.2. Invasive
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7. Conclusion
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Acknowledgement
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References
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Abstract
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Sponges are sessile benthic filter-feeding animals, which harbor numerous microorganisms. The
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enormous diversity and abundance of sponge associated bacteria envisages sponges as hot spots
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of microbial diversity and dynamics. Many theories were proposed on the ecological
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implications and mechanism of sponge-microbial association, among these, the biosynthesis of
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sponge derived bioactive molecules by the symbiotic bacteria is now well-indicated. This
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phenomenon however, is not exhibited by all marine sponges. Based on the available reports, it
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has been well established that the sponge associated microbial assemblages keep on changing
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continuously in response to environmental pressure and/or acquisition of microbes from
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surrounding seawater or associated macroorganisms. In this review, we have discussed
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nutritional association of sponges with its holobionts, interaction of sponges with other
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eukaryotic organisms, dynamics of sponge microbiome and sponge-specific microbial
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symbionts, sponge-coral association etc.
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Keywords: Sponges, microbial association, sponge-specific bacteria, ecological interactions
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1. Introduction
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Sponges are evolutionary ancient metazoans belonging to the phylum Porifera (Thakur and
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Muller, 2004). They are sessile organisms and are mainly found in marine and freshwater
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habitats (Kriska 2013; Pronzato et al., 2017). Sponges are highly efficient filter-feeding animals
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with porous internal canal system for circulating water throughout their body, providing nutrients
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as well as takes part in waste expulsion (Trautman and Hinde, 2001; Reiswig, 1974). About
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15,000 species of sponges have been described so far, but their true diversity may be higher
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(Hooper et al., 2002). There are mainly four classes of sponges namely the Calcarea (five orders
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and 24 families), Hexactinellida (six orders and 20 families), Homoscleromorpha (one order and
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two families) and Demospongiae (15 orders and 92 families), being the most populated class
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(Hooper et al., 2002; Gazave et al., 2012).
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Marine sponges are the main source of bioactive molecules from the marine environment (Blunt
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et al., 2004; Malve, 2016; Mehbub et al., 2014). The unique biosynthetic pathways of bioactive
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secondary metabolites derived from marine sponges are actually associated with sponge specific
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bacterial symbionts. It has been prooved that sponge derived bioactive molecules has been
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biosynthesized by sponge specific microbial symbionts (Sacristan-Soriano et al., 2011; Wilson et
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al., 2014). Sponges harbor a large population of microorganisms comprising about 50% of their
95
biomass (Hentschel et al., 2003, Usher et al., 2004a; Wang, 2006). Sponge tissues provide a
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dwelling place to many of the symbiotic species which include heterotrophic bacteria, facultative
97
anaerobes, dinoflagellates, cyanobacteria, archaea, yeast, fungi and even viruses (Webster and
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Hill, 2001; Schippers et al., 2012). Around 15,000 to 30,000 unique natural compounds have
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been isolated from marine sources (Arrieta et al., 2010; Mehbub et al., 2014; Malve, 2016; Kiuru
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et al., 2014; Lindequist, 2016). So far only few pharmaceutical products derived from sponges
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have been approved by FDA which include Cytarabine (Ara-C), vidarabine (Ara-A),
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Halichondrin B, Eribulin mesylate (a Halichondrin analogue) is the latest addition to these
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products (Huyck et al., 2011; Mayer et al., 2010; Montaser & Luesch, 2011; Jordan et al., 2005)
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Approval for marine drugs started with the drug zoconotide, a peptide derived from a tropical
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marine cone snail in 2004 which was used for the treatment of chronic pain caused from spinal
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cord injury (Perdicaris et al., 2013). Trabectedin is an anti-tumour compound extracted from sea-
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squirt for the first time in 2007. An example of bioactive compound that is produced by sponge
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is stevensine from Axinella corrugate; stevensine can be produced in primary sponge cell
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cultures. Halichondrin isolated from the sponge Lyssodendoryx has proven to possess strong
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anti-tumor effects. In the last few years, several extracts from marine environment are under
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Phase I-III trials (Mayer et al., 2010). Ara-C is documented as the first marine derived anticancer
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agent that has been recently used for the treatment of leukemia (Schwartsman, 2000; Proksch et
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al., 2002). Monanchocidin, a novel polycyclic guanidine alkaloid isolated from the marine
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sponge Monachora pulchra was found to induce cell death in human monocytic leukemia,
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human cervical cancer and mouse epidermal (Guzii at al., 2010). A novel cytotoxic peptide
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KENPVLSLVNGMF isolated and purified using enzyme mediated hydrolysis from the marine
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sponge Xestospongia testudinaria was found toexhibit significant cytotoxicity to thethe human
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cervical cancer cell line (HeLa) (Quah et al., 2017). Dimeric sphingolipid leucettamol A (1) was
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isolated for the first time along with 5, Bromophakelline (bromo pyrrole alkaloid) from the
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marine sponge Agelas sp. and acts as an anti-mycobacterial compound against Mycobacterium
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smegmatis (Abdjul et al., 2017). Ceylonins G–I: spongian diterpenes have been isolated from
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the marine sponge Spongia ceylonensis and have shown inhibitory activity against Ubiquitin-
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specific protease 7 (USP7) (El-Desoky et al., 2017). Microbes associated with marine sponges
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perform biological as well as ecological roles including nutrient cycling, synthesis of bioactive
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molecules such as antibiotics (Graçia et al.,2016), biosurfactants (Kiran et al., 2010), poly-
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hydroxy butyrates (Sathiyanarayana et al.,2013; Kiran et al.,2016), pigments (Ibrahim et al.,
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2014; Kiran et al., 2014), enzymes (Mohapatra et al., 2003; Shanmughapriya et al., 2009; Selvin
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et al., 2012), antipredation compounds (Kelman et al., 2009; Selvin et al., 2010) and antibiofilm
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compounds (Kiran et al., 2010; Stowe et al., 2011) that prevents predation and fouling (Satheesh
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et al., 2016). Various factors influencing sponge microbial associations include nutrient
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availability, water current, ecological niche and temperature (Simister et al., 2012).Though this
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review primarily intends to describe sponge associated unique microbial symbionts, an insight of
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eukaryotic symbionts was included in the review as to substantiate recent deliberations on
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recruitment of microbial symbionts from eukaryotic associates. Dynamics of sponge microbiome
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and sponge-coral association has also been discussed.
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2. Insights of sponge-eukaryotic symbionts
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Sponges have been associated with wide range of eukaryotic symbionts, however the
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exchange/acquisition of microbial symbionts from associated eukaryotes remains to be explored.
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Recent insights from coral-sponge association provide an evidence for the possible exchange of
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microbial symbionts in between the two. The researcher documented a list of sponge associated
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macroorganisms which include polychaetes, macroalgae, mangroves, barnacles, hydrozoans,
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anthozoans, ophiurids, insects, yeast, fungi and corals (Siepmann and Hoshnk, 1992; Holler et
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al., 2000; Avila et al., 2007).
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2.1. Sponge-algae symbiosis
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The Haliclona-Ceratodictyon association was reported as an obligate symbiosis and in this
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sponge-macroalgal symbiosis, neither sponge nor alga grow independently or in association with
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other species (Trautman et al., 2000). As the Haliclona caerulea/Jania adherens association has
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been reported as an obligatory and mutualistic association (Naim, 2015).
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2.2. Sponge- fungi symbiosis
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The investigation of fungal association with the sponge has been initiated through the molecular
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detection of the sponges namely Suberites zeteki and Mycale armata collected from Kaneohe
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Bay located on the northeastern coast of the island of Oahu, HI and reported more than 20 fungal
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species from each sponges. The fungal species reported includes Cladosporium sp, Hortaea sp,
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Aureobasidium sp, Penicillium sp, Aspergillus sp, Hypocreales sp, Gibberella sp, Candida sp,
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Ascomycota sp, Phoma sp under the phylum of Ascomycot and Schizophyllum sp, Phlebia sp,
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Malassezia sp, Basidiomycete sp under the phylum of Basidiomycota (Gao et al., 2008). The
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study has been continued with the traditional isolation method of fungal communities from
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sponge samples Amphimedon viridis, Axinella corrugate, Dragmacidon reticulate, Geo-dia
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corticostylifera, Mycale laxissima, Mycale angulosa and around 61 species have been isolated
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and grouped under the genus of Aspergillus, Agaricales, Atheliales, Acremonium, Arthtiniun,
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Bionectria, Botryosphaeria, Cunninghamela, Mucor, Nectria, Pestalotiopsis, Polyporales,
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Rhizopus,
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Trichoderma, Verticillium. However among the fungal communities, around 8-25% has been
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reported as unidentified cultures. It is worth to note that the fungal symbionts of sponges have
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the ability to tolerate the high salinity and pH and reported for its potential of lignocelluloses
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Cladosporium,
Cochliobolus,
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Glomerella,
Penicillium,
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degrading enzymes (Menezes et al., 2010). The fungus Scopulariopsis brevicaulis isolated from
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the sponge has been reported originally originated from the terrestrial soil (Kumar et al., 2015).
171 172•
2.3. Sponge- yeast symbiosis
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examination of egg and adult tissue. It believed to play an important role in sponge metabolism
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(Maldonado et al., 2005). The novel yeast isolate Leucosporidium escuderoi f.a., sp. nov., has
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been reported form the marine sponge Hymeniacidon sp collected from Fildes Bay, King
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George Island, Antarctica (Laich et al., 2014). This sponge yeast symbiosis and mechanisms of
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the yeast association has not been evaluated well.
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2.4. Sponge- polychaetes symbiosis
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The polychaetes are frequently found in close proximity to sponges due to the presence of holes,
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grooves, chambers and channels (Martin and Britayev, 1998) that shelter them as well as act as a
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good source for providing nutrients. Among the polychaetes, Haplosyllides has been reported to
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be an obligate endosymbiont of the sponge Xetospongia muta (Martin et al., 2008). Sponges are
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unique marine sedentary filter feeders not efficient in capturing prey size >5 µm (Sarda et al.,
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2002). Expulsion of such large food particles (prey) in filter feeding mechanism of sponges is an
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energy dependent process. The association of polychaete worms could be beneficial to the host
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sponges as the worms could prey such large organisms and the excreta of digested prey could be
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used as a nutritional source of host sponges (Sarda et al., 2002).
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2.5. Sponge- barnacles symbiosis
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Barnacles are the sedentary crustacean animals, commonly found in the intertidal and shallow
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subtidal zones of oceans. They exist as free-living as well assymbionts, and they
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principally cause marine fouling because of encrustation on ships and marine engineering
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devices. Symbiotic barnacles are found to be associated with various marine fauna starting from
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motile organisms such as whales, sirenians, sea turtles, crocodiles, sea snakes, crustaceans, and
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molluscs to sessile organisms including sponges, cnidarians and bryozoans. Ilan and co-workers
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reported that eight different species of barnacles residing in nine species of sponges surveyed
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from the Red Sea. As inferred by them, barnacles residing on sponges face the danger of being
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overgrown and engulfed by the host tissue (Ilan et al., 1999). Two sponge species Theonella
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conica and Callyspongia sp., are slow grower hence, less possibility to be engulfed. Although
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sponge-barnacle association has been reported as mutualistic, barnacles gain extra benefits, since
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The sponge Chondrilla nucula proved as a habitant for endosymbiotic fission yeast by the TEM
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the sponge (host) defense protects the barnacles from predation and competition (Van et al.,
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2010).
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2.6. Sponge- mangroves symbiosis
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Mangrove forests are considered as one of the most vegetated estuarine environments of the
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marine ecosystem as they comprise of several flora and fauna thriving in the nutrient limited,
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drenched and anoxic soils (Ellison et al., 1996). A transplantation study of Ellison and co-
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workers reported the facultative mutualism between the red mangrove Rhizophora mangle and
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its root-fouling sponges namely, Tedaniaignis and Haliclona implexiformis in the mangrove cays
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of Central America (Ellison et al., 1996). These root fouling sponges benefit the mangrove by
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facilitating the transfer of inorganic nitrogen to adventitious roots (Ellison et al., 1996). The
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ecological interaction between sponges and mangroves remains unclear and require
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comprehensive investigation. The study conducted by Hunting and co-workers concluded that
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the tannins play a vital role in recruitment of associated sponge Tedania ignis. The tannin and
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polyphenol production in roots of mangrove plant Rhizophora mangle and its responsibility for
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the sponge colonization were also reported. Since, it is being a suitable example of plant-animal
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symbiosis (Hunting et al., 2010).
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2.7. Sponge- other symbiosis
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Crocker and Reiswig reported that six species of common Caribbean Zoanthidea (Parazoanthus
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swiftii,
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and Epizoanthus sp.) were constrained to live on surfaces of reef-dwelling sponges (Crocker and
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Reiswig, 1981) Turon et al. (2000) reported the specific mass recruitment of Ophiothrix fragilis
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(Ophiuroidea) on sponges as commensals and the associated Ophiurids clean up the internal
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surfaces of the sponges (Hendler 1984; Turon et al., 2000). The aquatic insect Sisyrafuscata have
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been reported as a symbiotins with an European freshwater sponge, Euspongilla lacustris
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(Henry, 1967). Once associated with the sponge, the larva completes its life cycle within the
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sponge as the host provides it with food, shelter and oxygen (Henry, 1967). The association of
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demosponge Hymeniacidon perlevis with an edible mussel Mytilus galloprovincialis was
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reported recently (Longo et al., 2016). Sponges have been reported to be associated with
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hydrozoans (Puce et al., 2005) and other sponges as well. Wilcox and co-workers reported a
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symbiotic association between two sponges in the Florida Keys wherein the two-sponge species
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(Penares hellericovered by an external sponge, Antho involvens) were tough to take apart. The
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interesting phenomena to look into particularly, how their nutritional acquisition, ecology and
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evolution took place (Wilcox et al., 2002).
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3. Sponge-specific microbial symbionts
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Sponges hold highly diverse, yet specific microbial symbiont communities, despite the constant
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influx of seawater microorganisms resulting from their filter-feeding activities (Taylor et al.,
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2013; Thomas et al., 2016). Ecological perspectives of microbial symbionts associated with
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sponges have been considered as great importance as it seems to be a determinant of niche
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selection, biodiversity and biogeography.
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3.1. Functional ecology of symbiosis
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The microbial contribution towards the total weight of the sponge has been investigated
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continuously and reported as near as 50% of the sponge biomass (Hentschel et al., 2003;
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Hentschel et al., 2006; Schippers et al., 2012). Some of the proposed reasons for the maintenance
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of sponge-microbial symbiont association (Thacker and Freeman, 2012) include nutrient cycling,
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strengthening of sponge skeleton, recycling of metabolic wastes and synthesis of secondary
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metabolites to combat predation and fouling. Functional ecology and symbiotic interactions of
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microbes in sponges include nutritional benefits to the host sponge through nitrogen recycling
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(Bayer et al., 2008). The interaction between these symbionts and the host sponges has not been
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well understood yet as they may be invasive or beneficial (from parasitism to mutualism)
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(Thacker and Freeman, 2012). The available reports envisage the functional ecology of sponge-
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microbial association and can be grouped under two categories namely, chemical defense and
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nutritional symbiosis (Pawlik et al., 1995; Taylor et al., 2007a). Sponges have been reported in
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symbiotic relation with photosymbiotic cyanobacteria (Thacker, 2005) mimicking the
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dinoflagellate-coral symbiosis (Fournier, 2013).
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3.2. Sponge- bacterial symbiosis
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Sponges are known to associate with microorganisms spanning a remarkable number of different
257
microbial phyla and candidate phyla ranging between 41-60 (Taylor et al., 2007a; Schmitt et al.,
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2012; Reveillaud et al., 2014; Rix et al., 2016a; Thomas et al., 2016; Webster and Thomas, 2016;
259
Silva et al., 2017; Steinert et al., 2017). The levels of richness and diversity of these symbiont
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communities vary widely between sponge species, most of which are considered metabolically
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active (Kamke et al., 2010; Webster and Thomas, 2016). Phylogenetic analysis has revealed that
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the dominant sponge-associated microorganisms reside within the taxa Gamma- and
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Alphaproteobacteria, Actinobacteria, Chloroflexi, Nitrospirae, Cyanobacteria, Entotheonella the
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candidate phylum “Poribacteria,” “Thaumarchaea,” and ‘Tectobacteria’ (Hentschel., 2012;
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Simister et al., 2012, Wilson et al., 2014, Webster and Thomas, 2016). It has been hypothesized
266
that a combination of vertical and horizontal microbial transmission might be occurring in
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sponges leads to highly specific associations on the one hand and ensures global distributions on
268
the other (Hentschel., 2012). The relative abundance of sponge specific bacteria might be playing
269
an important role in the synthesis of secondary metabolites required for protection of host sponge
270
(Fig. 1). Perhaps sponge associated bacteria were highly abundant than sponge specific bacteria.
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There are some evidences surfacing which support that sponge specific bacteria may be involved
272
in the synthesis of sponge derived bioactive molecules (Mehbub et al., 2014).
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Through metagenomics, the functions of sponge bacteria including defence mechanisms,
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metabolic interactions with host through vitamin production, nutrient transport and utilization,
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redox sensing and protein-protein interactions mediated through ankyrin and tetratricopeptide
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repeat
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Gammaproteobacteria which are specific to sponges have a close homology to the ammonia-
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oxiding Nitrococcus clade, while phylotypes of Nitrosomonaseutropha/ europaeahave been
279
found commonly associated withvarious mangrove sponges (Diaz et al., 2004). Chloroflexiwas
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the one of the most common and diverse bacterial phyla in sponges and contains many sponge-
281
specific lineages.
282
The sponge Dendrilla nigracontains diverse bioactives including antibacterial, antifungal,
283
brineshrimp cytotoxicity, microalgal lethality, insecticidal, anticoagulant, anti-fouling and anti-
284
predation properties (Selvin and Lipton, 2004). To explore the associated bacteria to produce
285
bioactive metabolites and to understand the chemical ecology of host sponge, efforts were taken
286
for the successful isolation of antagonistic producers. Five media compositions including one
287
without enrichment (control), enriched with sponge extract, with growth regulator (antibiotic),
288
with auto inducers (such as cAMP and g-butyrolactone, an analogue of acyl homoserine
289
lactones, AHLs) and complete enrichment containing sponge extract, antibiotic and auto
290
inducers were developed. DNA hybridization assay was used to explore host specific bacteria
291
and ecotypes of culturable sponge associated bacteria. Enrichment with selective inducers (AHLs
292
and sponge extract) and regulators (antibiotics) considerably enhanced the cultivation potential
have
been
studied
(Fig.
2;
Thomas
et
al.,
2010).
The
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of sponge associated bacteria (Selvin, 2009; Esteves et al., 2016). The strain MSI051 was the
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first isolate obtained in the efforts for culturing the Candidatus (unculturable) heterotrophic
295
bacteria found associated with the marine sponge Dendrilla nigra. Based on the biochemical
296
characteristics and phylogenetic analysis, the strain MSI051 was named as Streptomyces dendra
297
since the isolate was an endosymbiont of D. nigra (Selvin, 2009).
298
3.3. Sponge- Actinobacteria symbiosis
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Actinobacteria associated with marine sponges are mostly secondary metabolite producers which
300
are used in natural products and drug discovery. The members of Acidimicrobiae are sponge
301
specific bacteria closely related to culturable Microthrix parvicella and Acidimicrobium
302
ferreoxidans. In the marine sponge Rhopaloeides odorabile, actinobacteria have been recovered
303
by using culture dependent and independent method (Webster et al., 2001). It has been
304
discovered that three sponge-specific actinobacterial clusters are found in Theonella swinhoei
305
and Aplysina aeropoba (Hentschel et al., 2002; Montalvo et al., 2005; Olson and Mccarthy,
306
2005). Recently, the new azepino-diindole alkaloid, rhodozepinone (1) has been isolated from
307
the marine sponge associated actinomycete Rhodococcus sp. UA13 and exhibited antibacterial
308
and anti-trypanosomal activity against S. aureus NCTC 8325, T. brucei brucei TC221, T. brucei
309
brucei TC221 (Elsayed et al., 2017).
310
3.4. Sponge- Cyanobacteria symbiosis
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Cyanobacteria represent the most mutual candidate of the sponge-associated microbial
312
communities. This symbiont functions in the host machinery as a manager of photosynthesis,
313
nitrogen fixation, light shielding and defense (Webster and Taylor, 2012). The evidence of algal-
314
sponge symbiosis was first reported by Vacelet (1981). The association of unicellular
315
cyanobacteria with sponges has been reported (Thacker, 2005) which provide nutritional
316
supplementation to its host thereby increasing biotic potential of sponges and growth. However,
317
the cyanobacterial symbionts gain benefit by living inside the host internal cavities to prevent
318
themselves from predation (Usher, 2008). Among the cyanobacteria, Synechococcus was
319
considered as the chief contributor of carbon fluxes to sponge (Usher, 2008). The Cyanobacteria,
320
Synechococcus or Prochlorococcus which were photosynthetic organisms were the single most
321
dominant species in world’s ocean.These photosynthetic organisms were found in 26
322
Demospongiae and 17 Calcarae families which were responsible for the characteristic colours in
323
sponge hosts. The colour variations in phycobiliprotein indicates the species of sponge host
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(Usher et al., 2004c). They were mostly found on the outer surfaces and distributed throughout
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the inner core of the sponges. The Aphanocapsa feldmannii, Synechococcus feldmannii- type
326
symbionts
327
Candidatus‘Synechococcus spongiarum’ was identified from the sponge Chondrilla nucula
328
(Usher et al. 2004b). The members of Synechococcus clade lacks co-speciation with their sponge
329
host. Filamentous cyanobacterium, Oscillatoria spongeliae found in many Dysidea sponges
330
exhibit a high level of host specificity harbouring its own symbiont strain than Synechococcus
331
(Thacker and Stranes, 2003; Ridley et al., 2005).In recent studies, the sponge specific bacteria
332
were also found to be present in other marine environments which originated from adult sponge
333
tissue through damage or release at reproductive stages (Taylor et al., 2013).
of
four
closely
related
lineages
(Usher
et
al.,
2004a).
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4. Nutritional association of sponges and its holobionts
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Sponges belong to the most ancient living Metazoa and generally develop symbiotic
337
relationships with complex communities of microorganisms (Taylor et al., 2007a; Hentschel et
338
al., 2012; Yin et al., 2015; Thomas et al., 2016).The framework of interconnected metabolisms
339
of all living beings still maintains the ecological balance of this earth through food web and
340
nutrient cycling which are obvious even in the marine ecosystem.
341
4.1. Sponge- holobiont symbiosis
342
In accordance with the holobiont concept (Bordenstein and Theis, 2015; Slaby et al., 2017), the
343
highly diverse symbiotic microbial communities of marine sponges are thought to play a crucial
344
role in their evolutionary success (Easson and Thacker, 2014; Tian et al., 2014; Webster and
345
Thomas, 2016; Slaby et al., 2017). The nutritional exchange between sponge and symbiont not
346
only impacts the individual benefits of the holobionts, but also to the environment where the
347
suspension-feeding activity of sponges cleans up the surrounding seawater. There is growing
348
interest in the nutrient fluxes within this holobiont as they equally influence the ecological and
349
biogeochemical sources. This is because the sponges almost directly determine the levels of
350
dissolved nutrients including carbon, nitrogen, silicates and so on for the primary production.
351
Microbial association of sponges mostly occurs in sponge mesohyl, but some were intracellular
352
symbionts (Maldonado et al., 2012). Many species are colonized by dense and diverse microbial
353
consortia that are present extracellularly within the mesohylmatrix (high microbial abundance)
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while other species are almost devoid of microorganisms (low microbial abundance) (Taylor et
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al.,2007a; Hentschel et al., 2012; Gloeckner et al., 2014; Ryu et al., 2016).
356
4.2. Nitrogen metabolism
357
Sponge symbionts also have a role in the nitrogen metabolism of their hosts, the presence of
358
nitrogen fixing bacteria in the Indo-Pacific coral reef sponge Callyspongia muricina was
359
described by (Wilkinson et al., 1999). Sponge-associated fungi have a significant role in the
360
nutrient recycling in their environment (Proksch et al., 2008; Colman, 2015). The association of
361
these fungi as obligate symbionts of these sponge species remains unclear. In a nutrient stress
362
condition, sponge associated bacteria effectively regulate nitrogenous wastes excreted from the
363
sponge host to maintain uptake of inorganic nitrogen (Fig. 3). Ammonia-oxidizing bacteria of the
364
genera Nitrosospira and Nitrosococcus (Mohamed et al., 2010) and the ammonia-oxidizing
365
archaea, such as candidatus Cenarchaeum symbiosum (Park et al., 2010) plays an important role
366
in the conversion of ammonia to nitrite in sponges. Nitrite oxidizing bacteria (NOB) such as
367
Nitrospinaand Nitrospira (Off et al., 2010; Feng et al., 2016) as well as denitrifying bacteria such
368
as Pseudovibrio denitrificans (Bondarev et al., 2013) have been identified in many sponge
369
species. In sponge associated bacteria, the assimilation of ammonia takes place through
370
glutamine synthase- glutamine oxoglutarate aminotransferase (GS-GOGAT) pathway (Fig. 2)
371
and the genes encoding for urease and urea transporters have been described (Hallam et al.,
372
2006; Siegl et al., 2011).
373
4.3. Carbon fixation
374
During the symbiotic association between sponges and microbes, the microbes use a variety of
375
sugar and carbon compounds from sponges for their nutritional benefits. Poribacteria are
376
involved in autotrophic carbon fixation which contain ATP- citrate lyase genes involved in the
377
reductive TCA cycle (Siegl et al., 2011). The sponge C. concentrica associated with
378
Deltaproteobacteria were found to have association with cyanobacteria (Hentschel et al., 2012).
379
Autotrophic carbon assimilation has been reported previously in Cenarchaeum symbiosum, a
380
crenarchaeota symbiotically associated with axinellid sponges (Hallam et al., 2006).
381
4.4. Other metabolism
382
Several species of boring sponges are found symbiotically associated with zooxanthellae and this
383
symbiotic association enhances the growth rate of the sponge via enhancing decalcification and
384
increasing boring capacity of the sponge (Hill et al., 1996). Creatine is synthesized by most of
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the invertebrates including sponges (Lavy et al., 2014), and can be converted in-vivo non-
386
enzymatically and irreversibly to creatinine by creatinase. Creatinase coding genes has been
387
found in sponge-associated bacteria from multiple sponge species, demonstrating the ability of
388
the sponge symbionts to degrade and use metabolic intermediates such as creatinine,
389
pyrimidines, or 5-oxoproline (Lavy et al., 2014).
390
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The sponge and the microbes interactby the presence of ankyrin repeat (AR) and TPR proteins
392
which mediate protein-protein interaction in eukaryotes (Fig. 2). These proteins are involved in
393
various functional processes like transcriptional initiators, cell cycle regulators, cytoskeleton
394
proteins, ion transporters and signal transducers (Thomas et al., 2010; Liu et al., 2011).The
395
putative sponge-specific bacterial family Poribacteria can produce methyl-branched fatty acids
396
(Hochmuth et al., 2010) and metabolic interactions are shared between the host Cymbastella
397
concentrica and its symbiont community (Thomas et al., 2010). There were several putative
398
host-interaction factors like Ig like domains and laminin G domain proteins which were involved
399
in adhesion and the presence of eukaryotic domains such as ankyrin, Sel1, fibronectin type III,
400
leucin-rich repeat. These proteins provide the information of host poribacterial interaction
401
(Taylor et al., 2007a; Taylor et al., 2007b)Ankryinsare important as theyare involved in the
402
recognition and protection from host phagocytosis (Liu et al., 2012).
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5. Dynamics of sponge microbiome
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Bacterial phyla which have been identified from sponges include, Acidobacteria, Actinobacteria,
406
Bacteroidetes,
407
Gemmatimonadetes, Nitrospira, Planctomycetes, Proteobacteria (Alpha, Beta, Delta and
408
Gammaproteobacteria), Spirochaetes, and Verrucomicrobia (Kim, 2015). In addition to these,
409
fluorescence in situ hybridization (FISH) studies showed the presence of Rhopaloeides odorabile
410
(Webster et al., 2001). Fusobacteria have been isolated from New Zealand sponge Stellata
411
maori, and it appears to be the only phylum present in that sponge (Schmitt et al., 2012).
412
Archaea reported from marine sponges include the members of the phylum Crenarchaeota with
413
a few from the phylum Euryarchaeota (Pesaro and Widmer, 2002; Zhang et al., 2015a).The
414
group Crenarchaeotais prominent in marine environments (Polonia et al., 2014). 16S rRNA gene
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Cyanobacteria,
Deinococcus-Thermus,
Firmicutes,
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415
library constructed from the freshwater sponge Spongilla lacustris provides sequences from the
416
Actinobacteria, Chloroflexi, and Alpha- and Beta-proteobacteria (Gernert et al., 2005).
417
Eukaryotic microbes were also reported to be present in sponges. In a recent study, sponge-
419
associated fungus, Truncatella angustata has been reported to produce Truncateols, a new
420
isoprenylated cyclohexanols with anti-H1N1 virus activities (Zhao et al., 2015). Limited
421
information is available as far as the sponge-associated viruses were concerned, while virus-like
422
particles have been observed in cell nuclei of Aplysina (Verongia) Cavernicola (Vacelet and
423
Gallissian, 1978). They may have a role to play in sponge cell pathology. In addition to the high
424
microbial diversity, more subtle patterns of host-symbiont distributions were recognized.
425
Sponges with high microbial abundance have been isolated from their different reproductive
426
stages as reported by Schmitt et al., (2008). The results from the previous studies prove the
427
unique existence of sponge-specific bacterial clusters (Schmitt et al., 2012).
428
5.1. Environmental factors
429
External environment conditions and host factors affect sponge microbial associations, but most
430
of the microbes are highly stable and resistant to physical and chemical agents. Starvation,
431
exposure to antibiotics, and even translocation of sponges such as Aplysina aerophoba (Friedrich
432
et al., 2001) and Aplysina cavernicola(Thoms et al., 2003) to different depths for brief periods
433
can cause only minor changes in their bacterial composition. Also, Aplysina fistularis which
434
wastranslocated from its natural depth of 4 m to an increased depth of 100 m showed no
435
significant changes in the cyanobacterial population (Maldonado and Young, 1998). In a recent
436
study conducted by Seo et al. (2016), bacterial profiling of three species of sponges namely,
437
Lubomirskia baicalensis, Baikalospongia intermedia and Swartschewskia papyracea by
438
pyrosequencing indicated abundance of Cyanobacteria. Diversity of the bacterial community in
439
S. papyracea was higher as compared to L. baicalensis and B. intermedia. Particularly, the
440
relative
441
2016). Thioautotrophic symbionts have been discovered from deep sea sponges like
442
Pachastrella sp. and share 99% sequence similarity with the thiosymbionts recovered from
443
poecilosclerid sponges and bathymodiolus mussels (Nishijima et al., 2010). However, elevation
444
of temperature causes a dominant shift in microbial community on marine sponges and also
445
decline in its health (Nishijima et al., 2010). A significant reduction in microbial population was
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abundance
of
Actinobacteria
was
higher
in
S.
papyracea
(Seo
et
al.,
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446
observed in the adult Rhopaloeides odorabilewhen the thermal threshold of 31–32ºC was slightly
447
shifted to 33ºC causing necrosis and loss of microbial symbionts (Simister et al., 2012).
448
Eutrophication causes significant changes in the diversity of the sponge-associated microbes
450
(Sabarathnam et al., 2010). It provides high influx of nutrients such as nitrogen and phosphorus,
451
which leads to increase in phytoplankton and bacterial populations which, in turn leads to a
452
higher biological oxygen demand (BOD) and increases the sedimentation rate of particulate
453
matter (Nogales et al., 2011). In contrast, Webster et al. (2014) reported that eutrophication had
454
no short-term effect on Cymbastela stipitata holobiont. (Luter et al., 2014).In earlier stages of
455
nutrient influx in Chesapeake Bay (Kan et al., 2008), bacterial communities were predominated
456
by SAR11, SAR86 and picocyanobacteria, however continued depletion of oxygen caused a shift
457
in the bacterial community to anaerobic members of the Firmicutes, Bacteroidetes and Sulphur-
458
oxidizing Gammaproteobacteria(West et al., 2016).The mechanisms of sponge microbial
459
associations are not well understood, but there were many theories that have beenproposed to
460
explain thesponge-microbial association. One of the theories suggestthat spongeduring its filter-
461
feeding selectively absorbs specific bacteria from the surrounding water containing
462
diversebacteria (Webster and Blackall, 2009). One more explanation is that there is a vertical
463
transmission of symbionts through the gametes of the sponge by inclusion of the bacteria in the
464
oocytes or larvae (Lee et al., 2009).
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6. Sponge-coral association: invasive or beneficial?
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Evolutionary link between sponge and coral reef has been increasing significance in
468
the functions of marine ecosystem. Sponges are playing a very important, beneficial role in
469
coral reef and ecosystem construction process, rather than destructive. Studies on the association
470
between sponge and corals are not well understood due to the difficulties in long term monitor,
471
sampling and follow-up, however, the maintaining the reef ecosystem dynamics is being obvious
472
beneficial role. Sponges are known to be facilitate corals in many ways including providing
473
nutrient (sponge loop), making suitable environment by clearing water and providing substrate
474
(stabilizing dead coral rubbles) for new recruits (Goreau and Hartman, 1963; Wulff and Buss,
475
1979; Rutzler, 2012; Rix et al., 2016a).
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477
6.1. Beneficial Food chain dynamics has important role in controlling the population and the whole
479
ecosystem dynamics (Fretwell, 1987). The dissolved organic carbon (DOC) plays a critically
480
role in carbon cycle. Sponges and corals work together and transfer the dissolved organic
481
matter to higher organisms in the form of food and the process is refereed as “sponge loop”.
482
In which sponge released DOC to water column trapped by the coral released mucus and
483
transferred to higher organisms (Rix et al., 2016a). This similar process confirmed through
484
laboratory isotope studies and observed in both shallow, warm water and deep sea cold water
485
corals reef system (Rix et al., 2016b). Recent study carried out at Florida Keys also supports
486
influence of sponge-derived DOM on chemical and ecological processes in coral reef ecosystems
487
(Fiore et al., 2017). Moreover, the research on sponge associated bacteria form granules evident
488
that microbes play a critical role in the phosphorus sequestration and phosphorous recycling in
489
the environment (Zhang et al., 2015b). As the research efforts are being taken worldwide to
490
understand complete functional role of this relationship for better conservation of the ecosystem.
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Apart from the nutritional exchange, filter feeding mechanism of sponges in water
492
column has also been play an important role in reef health by facilitating suitable environment
493
from turbid for corals to grow and reproduce. The quick recovery of reefs from turbid
494
environment caused by Hurricane was stated as best example and the studies carried out at
495
hurricane affected reefs at Florida Keys revealed the correlation between sponge abundance
496
(Filtering effects) and speedy recovery (Woodley et al., 1981). In addition, Mutualistic
497
association of sponge with corals also has been reported that, sponge gets space for growth
498
underneath the coral colonies, whereas the coral colony gets protected from bioeroders (Goreau
499
and Hartman, 1966; Hill, 1998). As an extra profit, exhalant water from sponge enhances the
500
food supply for corals that in turn increase coral growth, especially for coral polyps at the colony
501
edge next to the sponge (Wulff, 2012). Serious of studies carried out by Wulff (2012) clearly
502
highlighted the role that sponges can play in reef stabilization, consolidation and regeneration
503
(Wulff, 1984; 2001; 2012). The research work done by Rasser and Riegl (2002) revealed the
504
importance of sponge binding on Holocene coral reefs.
505
6.2. Invasive
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Although coral and sponges co-existed and maintain the balance in the marine
507
ecosystem for a very long period, there has been a report on coral sponge interaction and few
17
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reports on the short term impact to the coral communities (Jackson and Buss, 1975; Vicente,
509
1978; Suchanek et al., 1983). Several research studies indicates that, there were about 95
510
sponge species and 21 coral species engaged in sponge/coral interactions with minimal damage
511
to overgrown coral colonies (Aerts, 1998). Although, the sad thing about the association is few
512
sponge invasion and competitive succession over the corals has been increase and expanded
513
its geographical locations due to climate change and the anthropogenic stress (Bell et al.,
514
2013). In particular, the sponges such as Chondrilla nucula, Cliona spp. and Terpios hoshinota
515
were aggressively grown over live corals and killed (Hill, 1998; Suchanek et al., 1983; Liao et
516
al., 2007; Thinesh et al., 2015; 2017). However, the mechanism of this sponge association over
517
corals and factors which influence the sponge outbreak is poorly been understood.
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The coral killing sponge T. hoshinota, Terpios has been expanding its geographical
519
locations and cause mortality over 30 to 80% to many coral genera (Bryan, 1973). The invaded
520
reefs collected from American Samoa and Philippines (Plucer-Rosario, 1987), Japan (Rutzler
521
and Muzik, 1993; Reimer et al., 2011b), Taiwan (Liao et al., 2007), Great Barrier Reef in
522
Australia (Fujii et al., 2011), Indonesia (De voogd et al., 2013), recently in India (Thinesh et al.,
523
2015) and Mauritius (Elliott et al., 2016b). Atpresent, the sponge Terpios is being considered as
524
a “Nuisance Species” to coral reef ecosystem. Similarly, the Cliona sp. was also recorded as
525
abundance at coral reef environment (Ruzler, 2002: Schonberg and Ortiz 2008, Ward et al.,
526
2005; Kelmo et al., 2013).
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In Belize Cliona caribbaea covered two folds between 1979 and 1998 (Ruzler, 2002).
528
In Florida Keys the increasing trend has been noticed between 1996 and 2001 (Ward et al.,
529
2005). The similar trend was also recoded in Queen land reef of Australia between 1998 to
530
2004. Most of the invasive studies were done at a short period of time; hence, long term
531
assessment is the most important factor for the complete understanding of the effect. In terms
532
of understanding the mechanism for overgrowth of sponges, very few studies have been
533
attempted in Terpios. In accordance with the literature reported, the steps involved in the
534
mechanism of sponge invasion are summarized i) Dense populations of photosynthetic
535
cyanobacteria in the mesohyl could aid the sponge to enter into an active competition with
536
the corals, thereby leads to overgrowth by tendrils on the live corals (Wang et al., 2015; Elliott
537
et al.,2016a) ii) release of chemical deterrents to the ecosystem, leads the production of
538
cytotoxic compounds which weaken the coral tissue (Wang et al., 2015; Elliott et al., 2016a)
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539
iii) Tang et al. (2011), The changes in the microbial assemblages that accompany the invasion
540
process might weaken the coral and that resulted the sponge to attain succession during the
541
period of invasive growth. The exact ecological reason and the mechanism behind this invasive sponge outbreak
543
are remains unknown. However, the increasing evidence: Influence of ocean acidification,
544
climate change and pollution has the link to sponge outbreaks (Rutzler and Muzik, 1993;
545
Reimer et al., 2011b; Schils, 2012; Powell et al., 2014; Thinesh et al., 2017). On the hole, the
546
research studies and the long term co-existence of sponges in the healthy reef environment,
547
observed invasive impact most frequently at the sites where environmental conditions are
548
polluted and affected by climatic threats highlights the importance of sponges in the marine
549
ecosystem rather than destructive. Hence, further studies on the association particularly
550
nutritional exchange at different geographical locations with different environmental
551
conditions could provide valuable information to protect our ecosystem better.
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552
7. Conclusion
554
Marine sponges are sedentary aquatic animals harboring microbial symbionts upto 50% of
555
sponge biomass. Sponge-microbial association is a subject of investigation since unique
556
beneficial effects of host-symbionts remain unresolved. Albeit reports evident that sponge-
557
specific symbionts are responsible for synthesis and sequestration of sponge-derived bioactive
558
molecules, it has been reported that the sponge-microbiome consortia are not consistent in
559
different niches and geographical locations.The concept of microbiome dynamics, particularly
560
change of diverse sponge microbiome to specific abundant microbiome for the synthesis of
561
bioactive molecules, perhaps occurred as a response to external pressure such as predation or
562
competition and it should be mainstream focus of sponge microbiome research. The available
563
literature does not have any conclusive data to show the recruitment/exchange of microbial
564
symbionts between sponge and associated macroorganisms. The nutritional exchange between
565
sponge and microbial symbiont is illustrated in this review as an ecological benefit of sponge
566
microbial association. The symbiotic microbes play a significant role in the nutrient recycling of
567
sponge excreta and availability of nutrient in the surrounding seawater facilitate abundance of
568
planktonic organisms. Most of the available literature on sponge-coral association explains
569
invasive nature of sponges, but in situ shading-experiments have proven that changes in the
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570
microbial assemblage of sponge would reduce the colorization capacity over corals. However
571
further research is warranted on microbiome dynamics and symbiont acquisition which would
572
reveal unique symbiotic interactions.
573
Acknowledgements:
575 576 577 578
Authors are thankful to DBT, New Delhi for financial support. Authors SS & PR also thankful to University Grants Commission (UGC) for providing financial assistance in the form of Postdoctoral fellowship.
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Zhang, F., Blasiak, L.C., Karolin, J.O., Powell, R.J., Geddes, C.D., Hill, R.T., 2015b. Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. PNAS, 112 (14), 4381-4386. Zhao, Y., Si, L., Liu, D., Proksch, P., Proksch, P., Zhou, D., Lin, D., 2015. Truncateols A–N, new isoprenylatedcyclohexanols from the sponge-associated fungus Truncatellaangustata with anti-H 1 N 1 virus activities. Tetrahedron. 71,2708-2718.
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Figure legends
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Fig. 1. Interactions of holobionts and host sponge. Holobionts secret quorum sensing (QS)
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molecules (bioluminescence – lux, acyl homoserine lactones – AHL, rhamnolipids – RHL,
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biosurfactants etc.) for recruitment and selection of host specific holobionts and storage
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molecules like poly-hydroxy alkanoates – PHA for survival of holobionts in nutrient limited
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sponge niche. Host sponge offers shelter to the holobionts whereas holobionts secrete
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phospholipase A2 – PLA2 for synergistic host defense and bioactive molecules for host’s
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protection against pathogens, predation and fouling.
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Fig. 2. Ecological interactions and functional roles of sponge associated holobionts
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Fig. 3. Nitrogen fixation in marine sponges (Microorganisms involved have not been yet
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identified completely)
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Fig. 4. Sponge-coral association may be invasive to corals. But the functional roles and
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ecological interactions including recruitment of holobionts still remains to be explored
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Intends to describe sponge associated unique microbial symbionts An insight of eukaryotic symbionts-fungi, yeast etc., Visualization of coral killing sponge T. hoshinota, Terpios Influence of environmental factors on sponge association
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• • • •
S0141-1136(17)30668-2
DOI:
10.1016/j.marenvres.2018.04.017
Reference:
MERE 4513
To appear in:
Marine Environmental Research
Received Date: 2 November 2017 Revised Date:
1 March 2018
Accepted Date: 25 April 2018
Please cite this article as: Kiran, G.S., Sekar, S., Ramasamy, P., Thinesh, T., Hassan, S., Lipton, A.N., Ninawe, A.S., Selvin, J., Marine sponge microbial association: Towards disclosing unique symbiotic interactions, Marine Environmental Research (2018), doi: 10.1016/j.marenvres.2018.04.017. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Marine sponge microbial association: towards disclosing unique symbiotic interactions
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G. Seghal Kirana, Sivasankari Sekarb, Pasiyappazham Ramasamyb, Thangadurai Thineshc, Saqib Hassanb, Anuj Nishanth Liptonb, A.S. Ninawed, Joseph Selvinb*
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b
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Florida International University, Miami, Florida - 33199
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Department of Biotechnology, Ministry of Science and Technology, New Delhi, India
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*Corresponding author (J. Selvin):
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Department of Microbiology, School of Life Sciences, Pondicherry University, Puducherry –
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605014, India. Email: [email protected], [email protected]
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Department of Food Science and Technology, Pondicherry University, Puducherry – 605014, India.
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Department of Microbiology, School of Life Sciences, Pondicherry University, Puducherry – 605014, India
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1. Introduction
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2. Insights of sponge-eukaryotic symbionts
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2.1. Sponge-algae symbiosis
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2.2. Sponge- fungi symbiosis
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2.3. Sponge- yeast symbiosis
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2.4. Sponge- polychaetes symbiosis
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2.5. Sponge- barnacles symbiosis
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2.6. Sponge- mangroves symbiosis
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2.7. Sponge- other symbiosis 3. Sponge-specific microbial symbionts
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3.1. Functional ecology of symbiosis
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3.2. Sponge- bacterial symbiosis
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3.3. Sponge- Actinobacteria symbiosis
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3.4. Sponge- Cyanobacteria symbiosis
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Contents
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4. Nutritional association of sponges and its holobionts
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4.1. Sponge- holobiont symbiosis
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4.2. Nitrogen metabolism
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4.3. Carbon fixation
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4.4. Other metabolism
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5. Dynamics of sponge microbiome
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5.1. Environmental factors
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6. Sponge-coral association: invasive or beneficial?
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6.1. Beneficial
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6.2. Invasive
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7. Conclusion
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Acknowledgement
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References
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Abstract
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Sponges are sessile benthic filter-feeding animals, which harbor numerous microorganisms. The
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enormous diversity and abundance of sponge associated bacteria envisages sponges as hot spots
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of microbial diversity and dynamics. Many theories were proposed on the ecological
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implications and mechanism of sponge-microbial association, among these, the biosynthesis of
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sponge derived bioactive molecules by the symbiotic bacteria is now well-indicated. This
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phenomenon however, is not exhibited by all marine sponges. Based on the available reports, it
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has been well established that the sponge associated microbial assemblages keep on changing
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continuously in response to environmental pressure and/or acquisition of microbes from
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surrounding seawater or associated macroorganisms. In this review, we have discussed
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nutritional association of sponges with its holobionts, interaction of sponges with other
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eukaryotic organisms, dynamics of sponge microbiome and sponge-specific microbial
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symbionts, sponge-coral association etc.
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Keywords: Sponges, microbial association, sponge-specific bacteria, ecological interactions
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1. Introduction
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Sponges are evolutionary ancient metazoans belonging to the phylum Porifera (Thakur and
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Muller, 2004). They are sessile organisms and are mainly found in marine and freshwater
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habitats (Kriska 2013; Pronzato et al., 2017). Sponges are highly efficient filter-feeding animals
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with porous internal canal system for circulating water throughout their body, providing nutrients
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as well as takes part in waste expulsion (Trautman and Hinde, 2001; Reiswig, 1974). About
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15,000 species of sponges have been described so far, but their true diversity may be higher
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(Hooper et al., 2002). There are mainly four classes of sponges namely the Calcarea (five orders
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and 24 families), Hexactinellida (six orders and 20 families), Homoscleromorpha (one order and
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two families) and Demospongiae (15 orders and 92 families), being the most populated class
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(Hooper et al., 2002; Gazave et al., 2012).
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Marine sponges are the main source of bioactive molecules from the marine environment (Blunt
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et al., 2004; Malve, 2016; Mehbub et al., 2014). The unique biosynthetic pathways of bioactive
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secondary metabolites derived from marine sponges are actually associated with sponge specific
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bacterial symbionts. It has been prooved that sponge derived bioactive molecules has been
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biosynthesized by sponge specific microbial symbionts (Sacristan-Soriano et al., 2011; Wilson et
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al., 2014). Sponges harbor a large population of microorganisms comprising about 50% of their
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biomass (Hentschel et al., 2003, Usher et al., 2004a; Wang, 2006). Sponge tissues provide a
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dwelling place to many of the symbiotic species which include heterotrophic bacteria, facultative
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anaerobes, dinoflagellates, cyanobacteria, archaea, yeast, fungi and even viruses (Webster and
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Hill, 2001; Schippers et al., 2012). Around 15,000 to 30,000 unique natural compounds have
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been isolated from marine sources (Arrieta et al., 2010; Mehbub et al., 2014; Malve, 2016; Kiuru
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et al., 2014; Lindequist, 2016). So far only few pharmaceutical products derived from sponges
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have been approved by FDA which include Cytarabine (Ara-C), vidarabine (Ara-A),
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Halichondrin B, Eribulin mesylate (a Halichondrin analogue) is the latest addition to these
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products (Huyck et al., 2011; Mayer et al., 2010; Montaser & Luesch, 2011; Jordan et al., 2005)
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Approval for marine drugs started with the drug zoconotide, a peptide derived from a tropical
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marine cone snail in 2004 which was used for the treatment of chronic pain caused from spinal
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cord injury (Perdicaris et al., 2013). Trabectedin is an anti-tumour compound extracted from sea-
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squirt for the first time in 2007. An example of bioactive compound that is produced by sponge
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is stevensine from Axinella corrugate; stevensine can be produced in primary sponge cell
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cultures. Halichondrin isolated from the sponge Lyssodendoryx has proven to possess strong
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anti-tumor effects. In the last few years, several extracts from marine environment are under
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Phase I-III trials (Mayer et al., 2010). Ara-C is documented as the first marine derived anticancer
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agent that has been recently used for the treatment of leukemia (Schwartsman, 2000; Proksch et
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al., 2002). Monanchocidin, a novel polycyclic guanidine alkaloid isolated from the marine
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sponge Monachora pulchra was found to induce cell death in human monocytic leukemia,
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human cervical cancer and mouse epidermal (Guzii at al., 2010). A novel cytotoxic peptide
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KENPVLSLVNGMF isolated and purified using enzyme mediated hydrolysis from the marine
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sponge Xestospongia testudinaria was found toexhibit significant cytotoxicity to thethe human
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cervical cancer cell line (HeLa) (Quah et al., 2017). Dimeric sphingolipid leucettamol A (1) was
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isolated for the first time along with 5, Bromophakelline (bromo pyrrole alkaloid) from the
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marine sponge Agelas sp. and acts as an anti-mycobacterial compound against Mycobacterium
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smegmatis (Abdjul et al., 2017). Ceylonins G–I: spongian diterpenes have been isolated from
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the marine sponge Spongia ceylonensis and have shown inhibitory activity against Ubiquitin-
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specific protease 7 (USP7) (El-Desoky et al., 2017). Microbes associated with marine sponges
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perform biological as well as ecological roles including nutrient cycling, synthesis of bioactive
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molecules such as antibiotics (Graçia et al.,2016), biosurfactants (Kiran et al., 2010), poly-
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hydroxy butyrates (Sathiyanarayana et al.,2013; Kiran et al.,2016), pigments (Ibrahim et al.,
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2014; Kiran et al., 2014), enzymes (Mohapatra et al., 2003; Shanmughapriya et al., 2009; Selvin
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et al., 2012), antipredation compounds (Kelman et al., 2009; Selvin et al., 2010) and antibiofilm
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compounds (Kiran et al., 2010; Stowe et al., 2011) that prevents predation and fouling (Satheesh
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et al., 2016). Various factors influencing sponge microbial associations include nutrient
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availability, water current, ecological niche and temperature (Simister et al., 2012).Though this
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review primarily intends to describe sponge associated unique microbial symbionts, an insight of
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eukaryotic symbionts was included in the review as to substantiate recent deliberations on
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recruitment of microbial symbionts from eukaryotic associates. Dynamics of sponge microbiome
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and sponge-coral association has also been discussed.
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2. Insights of sponge-eukaryotic symbionts
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Sponges have been associated with wide range of eukaryotic symbionts, however the
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exchange/acquisition of microbial symbionts from associated eukaryotes remains to be explored.
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Recent insights from coral-sponge association provide an evidence for the possible exchange of
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microbial symbionts in between the two. The researcher documented a list of sponge associated
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macroorganisms which include polychaetes, macroalgae, mangroves, barnacles, hydrozoans,
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anthozoans, ophiurids, insects, yeast, fungi and corals (Siepmann and Hoshnk, 1992; Holler et
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al., 2000; Avila et al., 2007).
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2.1. Sponge-algae symbiosis
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The Haliclona-Ceratodictyon association was reported as an obligate symbiosis and in this
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sponge-macroalgal symbiosis, neither sponge nor alga grow independently or in association with
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other species (Trautman et al., 2000). As the Haliclona caerulea/Jania adherens association has
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been reported as an obligatory and mutualistic association (Naim, 2015).
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2.2. Sponge- fungi symbiosis
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The investigation of fungal association with the sponge has been initiated through the molecular
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detection of the sponges namely Suberites zeteki and Mycale armata collected from Kaneohe
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Bay located on the northeastern coast of the island of Oahu, HI and reported more than 20 fungal
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species from each sponges. The fungal species reported includes Cladosporium sp, Hortaea sp,
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Aureobasidium sp, Penicillium sp, Aspergillus sp, Hypocreales sp, Gibberella sp, Candida sp,
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Ascomycota sp, Phoma sp under the phylum of Ascomycot and Schizophyllum sp, Phlebia sp,
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Malassezia sp, Basidiomycete sp under the phylum of Basidiomycota (Gao et al., 2008). The
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study has been continued with the traditional isolation method of fungal communities from
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sponge samples Amphimedon viridis, Axinella corrugate, Dragmacidon reticulate, Geo-dia
162
corticostylifera, Mycale laxissima, Mycale angulosa and around 61 species have been isolated
163
and grouped under the genus of Aspergillus, Agaricales, Atheliales, Acremonium, Arthtiniun,
164
Bionectria, Botryosphaeria, Cunninghamela, Mucor, Nectria, Pestalotiopsis, Polyporales,
165
Rhizopus,
166
Trichoderma, Verticillium. However among the fungal communities, around 8-25% has been
167
reported as unidentified cultures. It is worth to note that the fungal symbionts of sponges have
168
the ability to tolerate the high salinity and pH and reported for its potential of lignocelluloses
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Cladosporium,
Cochliobolus,
Fusarium,
Glomerella,
Penicillium,
Phoma,
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169
degrading enzymes (Menezes et al., 2010). The fungus Scopulariopsis brevicaulis isolated from
170
the sponge has been reported originally originated from the terrestrial soil (Kumar et al., 2015).
171 172•
2.3. Sponge- yeast symbiosis
173
examination of egg and adult tissue. It believed to play an important role in sponge metabolism
174
(Maldonado et al., 2005). The novel yeast isolate Leucosporidium escuderoi f.a., sp. nov., has
175
been reported form the marine sponge Hymeniacidon sp collected from Fildes Bay, King
176
George Island, Antarctica (Laich et al., 2014). This sponge yeast symbiosis and mechanisms of
177
the yeast association has not been evaluated well.
178
2.4. Sponge- polychaetes symbiosis
179
The polychaetes are frequently found in close proximity to sponges due to the presence of holes,
180
grooves, chambers and channels (Martin and Britayev, 1998) that shelter them as well as act as a
181
good source for providing nutrients. Among the polychaetes, Haplosyllides has been reported to
182
be an obligate endosymbiont of the sponge Xetospongia muta (Martin et al., 2008). Sponges are
183
unique marine sedentary filter feeders not efficient in capturing prey size >5 µm (Sarda et al.,
184
2002). Expulsion of such large food particles (prey) in filter feeding mechanism of sponges is an
185
energy dependent process. The association of polychaete worms could be beneficial to the host
186
sponges as the worms could prey such large organisms and the excreta of digested prey could be
187
used as a nutritional source of host sponges (Sarda et al., 2002).
188
2.5. Sponge- barnacles symbiosis
189
Barnacles are the sedentary crustacean animals, commonly found in the intertidal and shallow
190
subtidal zones of oceans. They exist as free-living as well assymbionts, and they
191
principally cause marine fouling because of encrustation on ships and marine engineering
192
devices. Symbiotic barnacles are found to be associated with various marine fauna starting from
193
motile organisms such as whales, sirenians, sea turtles, crocodiles, sea snakes, crustaceans, and
194
molluscs to sessile organisms including sponges, cnidarians and bryozoans. Ilan and co-workers
195
reported that eight different species of barnacles residing in nine species of sponges surveyed
196
from the Red Sea. As inferred by them, barnacles residing on sponges face the danger of being
197
overgrown and engulfed by the host tissue (Ilan et al., 1999). Two sponge species Theonella
198
conica and Callyspongia sp., are slow grower hence, less possibility to be engulfed. Although
199
sponge-barnacle association has been reported as mutualistic, barnacles gain extra benefits, since
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The sponge Chondrilla nucula proved as a habitant for endosymbiotic fission yeast by the TEM
7
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the sponge (host) defense protects the barnacles from predation and competition (Van et al.,
201
2010).
202
2.6. Sponge- mangroves symbiosis
203
Mangrove forests are considered as one of the most vegetated estuarine environments of the
204
marine ecosystem as they comprise of several flora and fauna thriving in the nutrient limited,
205
drenched and anoxic soils (Ellison et al., 1996). A transplantation study of Ellison and co-
206
workers reported the facultative mutualism between the red mangrove Rhizophora mangle and
207
its root-fouling sponges namely, Tedaniaignis and Haliclona implexiformis in the mangrove cays
208
of Central America (Ellison et al., 1996). These root fouling sponges benefit the mangrove by
209
facilitating the transfer of inorganic nitrogen to adventitious roots (Ellison et al., 1996). The
210
ecological interaction between sponges and mangroves remains unclear and require
211
comprehensive investigation. The study conducted by Hunting and co-workers concluded that
212
the tannins play a vital role in recruitment of associated sponge Tedania ignis. The tannin and
213
polyphenol production in roots of mangrove plant Rhizophora mangle and its responsibility for
214
the sponge colonization were also reported. Since, it is being a suitable example of plant-animal
215
symbiosis (Hunting et al., 2010).
216
2.7. Sponge- other symbiosis
217
Crocker and Reiswig reported that six species of common Caribbean Zoanthidea (Parazoanthus
218
swiftii,
219
and Epizoanthus sp.) were constrained to live on surfaces of reef-dwelling sponges (Crocker and
220
Reiswig, 1981) Turon et al. (2000) reported the specific mass recruitment of Ophiothrix fragilis
221
(Ophiuroidea) on sponges as commensals and the associated Ophiurids clean up the internal
222
surfaces of the sponges (Hendler 1984; Turon et al., 2000). The aquatic insect Sisyrafuscata have
223
been reported as a symbiotins with an European freshwater sponge, Euspongilla lacustris
224
(Henry, 1967). Once associated with the sponge, the larva completes its life cycle within the
225
sponge as the host provides it with food, shelter and oxygen (Henry, 1967). The association of
226
demosponge Hymeniacidon perlevis with an edible mussel Mytilus galloprovincialis was
227
reported recently (Longo et al., 2016). Sponges have been reported to be associated with
228
hydrozoans (Puce et al., 2005) and other sponges as well. Wilcox and co-workers reported a
229
symbiotic association between two sponges in the Florida Keys wherein the two-sponge species
230
(Penares hellericovered by an external sponge, Antho involvens) were tough to take apart. The
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parasiticus,
P.
catenularis,
P.
puertoricense,
Epizoanthus
cutressi,
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interesting phenomena to look into particularly, how their nutritional acquisition, ecology and
232
evolution took place (Wilcox et al., 2002).
233
3. Sponge-specific microbial symbionts
235
Sponges hold highly diverse, yet specific microbial symbiont communities, despite the constant
236
influx of seawater microorganisms resulting from their filter-feeding activities (Taylor et al.,
237
2013; Thomas et al., 2016). Ecological perspectives of microbial symbionts associated with
238
sponges have been considered as great importance as it seems to be a determinant of niche
239
selection, biodiversity and biogeography.
240
3.1. Functional ecology of symbiosis
241
The microbial contribution towards the total weight of the sponge has been investigated
242
continuously and reported as near as 50% of the sponge biomass (Hentschel et al., 2003;
243
Hentschel et al., 2006; Schippers et al., 2012). Some of the proposed reasons for the maintenance
244
of sponge-microbial symbiont association (Thacker and Freeman, 2012) include nutrient cycling,
245
strengthening of sponge skeleton, recycling of metabolic wastes and synthesis of secondary
246
metabolites to combat predation and fouling. Functional ecology and symbiotic interactions of
247
microbes in sponges include nutritional benefits to the host sponge through nitrogen recycling
248
(Bayer et al., 2008). The interaction between these symbionts and the host sponges has not been
249
well understood yet as they may be invasive or beneficial (from parasitism to mutualism)
250
(Thacker and Freeman, 2012). The available reports envisage the functional ecology of sponge-
251
microbial association and can be grouped under two categories namely, chemical defense and
252
nutritional symbiosis (Pawlik et al., 1995; Taylor et al., 2007a). Sponges have been reported in
253
symbiotic relation with photosymbiotic cyanobacteria (Thacker, 2005) mimicking the
254
dinoflagellate-coral symbiosis (Fournier, 2013).
255
3.2. Sponge- bacterial symbiosis
256
Sponges are known to associate with microorganisms spanning a remarkable number of different
257
microbial phyla and candidate phyla ranging between 41-60 (Taylor et al., 2007a; Schmitt et al.,
258
2012; Reveillaud et al., 2014; Rix et al., 2016a; Thomas et al., 2016; Webster and Thomas, 2016;
259
Silva et al., 2017; Steinert et al., 2017). The levels of richness and diversity of these symbiont
260
communities vary widely between sponge species, most of which are considered metabolically
261
active (Kamke et al., 2010; Webster and Thomas, 2016). Phylogenetic analysis has revealed that
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the dominant sponge-associated microorganisms reside within the taxa Gamma- and
263
Alphaproteobacteria, Actinobacteria, Chloroflexi, Nitrospirae, Cyanobacteria, Entotheonella the
264
candidate phylum “Poribacteria,” “Thaumarchaea,” and ‘Tectobacteria’ (Hentschel., 2012;
265
Simister et al., 2012, Wilson et al., 2014, Webster and Thomas, 2016). It has been hypothesized
266
that a combination of vertical and horizontal microbial transmission might be occurring in
267
sponges leads to highly specific associations on the one hand and ensures global distributions on
268
the other (Hentschel., 2012). The relative abundance of sponge specific bacteria might be playing
269
an important role in the synthesis of secondary metabolites required for protection of host sponge
270
(Fig. 1). Perhaps sponge associated bacteria were highly abundant than sponge specific bacteria.
271
There are some evidences surfacing which support that sponge specific bacteria may be involved
272
in the synthesis of sponge derived bioactive molecules (Mehbub et al., 2014).
273
Through metagenomics, the functions of sponge bacteria including defence mechanisms,
274
metabolic interactions with host through vitamin production, nutrient transport and utilization,
275
redox sensing and protein-protein interactions mediated through ankyrin and tetratricopeptide
276
repeat
277
Gammaproteobacteria which are specific to sponges have a close homology to the ammonia-
278
oxiding Nitrococcus clade, while phylotypes of Nitrosomonaseutropha/ europaeahave been
279
found commonly associated withvarious mangrove sponges (Diaz et al., 2004). Chloroflexiwas
280
the one of the most common and diverse bacterial phyla in sponges and contains many sponge-
281
specific lineages.
282
The sponge Dendrilla nigracontains diverse bioactives including antibacterial, antifungal,
283
brineshrimp cytotoxicity, microalgal lethality, insecticidal, anticoagulant, anti-fouling and anti-
284
predation properties (Selvin and Lipton, 2004). To explore the associated bacteria to produce
285
bioactive metabolites and to understand the chemical ecology of host sponge, efforts were taken
286
for the successful isolation of antagonistic producers. Five media compositions including one
287
without enrichment (control), enriched with sponge extract, with growth regulator (antibiotic),
288
with auto inducers (such as cAMP and g-butyrolactone, an analogue of acyl homoserine
289
lactones, AHLs) and complete enrichment containing sponge extract, antibiotic and auto
290
inducers were developed. DNA hybridization assay was used to explore host specific bacteria
291
and ecotypes of culturable sponge associated bacteria. Enrichment with selective inducers (AHLs
292
and sponge extract) and regulators (antibiotics) considerably enhanced the cultivation potential
have
been
studied
(Fig.
2;
Thomas
et
al.,
2010).
The
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of sponge associated bacteria (Selvin, 2009; Esteves et al., 2016). The strain MSI051 was the
294
first isolate obtained in the efforts for culturing the Candidatus (unculturable) heterotrophic
295
bacteria found associated with the marine sponge Dendrilla nigra. Based on the biochemical
296
characteristics and phylogenetic analysis, the strain MSI051 was named as Streptomyces dendra
297
since the isolate was an endosymbiont of D. nigra (Selvin, 2009).
298
3.3. Sponge- Actinobacteria symbiosis
299
Actinobacteria associated with marine sponges are mostly secondary metabolite producers which
300
are used in natural products and drug discovery. The members of Acidimicrobiae are sponge
301
specific bacteria closely related to culturable Microthrix parvicella and Acidimicrobium
302
ferreoxidans. In the marine sponge Rhopaloeides odorabile, actinobacteria have been recovered
303
by using culture dependent and independent method (Webster et al., 2001). It has been
304
discovered that three sponge-specific actinobacterial clusters are found in Theonella swinhoei
305
and Aplysina aeropoba (Hentschel et al., 2002; Montalvo et al., 2005; Olson and Mccarthy,
306
2005). Recently, the new azepino-diindole alkaloid, rhodozepinone (1) has been isolated from
307
the marine sponge associated actinomycete Rhodococcus sp. UA13 and exhibited antibacterial
308
and anti-trypanosomal activity against S. aureus NCTC 8325, T. brucei brucei TC221, T. brucei
309
brucei TC221 (Elsayed et al., 2017).
310
3.4. Sponge- Cyanobacteria symbiosis
311
Cyanobacteria represent the most mutual candidate of the sponge-associated microbial
312
communities. This symbiont functions in the host machinery as a manager of photosynthesis,
313
nitrogen fixation, light shielding and defense (Webster and Taylor, 2012). The evidence of algal-
314
sponge symbiosis was first reported by Vacelet (1981). The association of unicellular
315
cyanobacteria with sponges has been reported (Thacker, 2005) which provide nutritional
316
supplementation to its host thereby increasing biotic potential of sponges and growth. However,
317
the cyanobacterial symbionts gain benefit by living inside the host internal cavities to prevent
318
themselves from predation (Usher, 2008). Among the cyanobacteria, Synechococcus was
319
considered as the chief contributor of carbon fluxes to sponge (Usher, 2008). The Cyanobacteria,
320
Synechococcus or Prochlorococcus which were photosynthetic organisms were the single most
321
dominant species in world’s ocean.These photosynthetic organisms were found in 26
322
Demospongiae and 17 Calcarae families which were responsible for the characteristic colours in
323
sponge hosts. The colour variations in phycobiliprotein indicates the species of sponge host
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324
(Usher et al., 2004c). They were mostly found on the outer surfaces and distributed throughout
325
the inner core of the sponges. The Aphanocapsa feldmannii, Synechococcus feldmannii- type
326
symbionts
327
Candidatus‘Synechococcus spongiarum’ was identified from the sponge Chondrilla nucula
328
(Usher et al. 2004b). The members of Synechococcus clade lacks co-speciation with their sponge
329
host. Filamentous cyanobacterium, Oscillatoria spongeliae found in many Dysidea sponges
330
exhibit a high level of host specificity harbouring its own symbiont strain than Synechococcus
331
(Thacker and Stranes, 2003; Ridley et al., 2005).In recent studies, the sponge specific bacteria
332
were also found to be present in other marine environments which originated from adult sponge
333
tissue through damage or release at reproductive stages (Taylor et al., 2013).
of
four
closely
related
lineages
(Usher
et
al.,
2004a).
The
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4. Nutritional association of sponges and its holobionts
336
Sponges belong to the most ancient living Metazoa and generally develop symbiotic
337
relationships with complex communities of microorganisms (Taylor et al., 2007a; Hentschel et
338
al., 2012; Yin et al., 2015; Thomas et al., 2016).The framework of interconnected metabolisms
339
of all living beings still maintains the ecological balance of this earth through food web and
340
nutrient cycling which are obvious even in the marine ecosystem.
341
4.1. Sponge- holobiont symbiosis
342
In accordance with the holobiont concept (Bordenstein and Theis, 2015; Slaby et al., 2017), the
343
highly diverse symbiotic microbial communities of marine sponges are thought to play a crucial
344
role in their evolutionary success (Easson and Thacker, 2014; Tian et al., 2014; Webster and
345
Thomas, 2016; Slaby et al., 2017). The nutritional exchange between sponge and symbiont not
346
only impacts the individual benefits of the holobionts, but also to the environment where the
347
suspension-feeding activity of sponges cleans up the surrounding seawater. There is growing
348
interest in the nutrient fluxes within this holobiont as they equally influence the ecological and
349
biogeochemical sources. This is because the sponges almost directly determine the levels of
350
dissolved nutrients including carbon, nitrogen, silicates and so on for the primary production.
351
Microbial association of sponges mostly occurs in sponge mesohyl, but some were intracellular
352
symbionts (Maldonado et al., 2012). Many species are colonized by dense and diverse microbial
353
consortia that are present extracellularly within the mesohylmatrix (high microbial abundance)
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while other species are almost devoid of microorganisms (low microbial abundance) (Taylor et
355
al.,2007a; Hentschel et al., 2012; Gloeckner et al., 2014; Ryu et al., 2016).
356
4.2. Nitrogen metabolism
357
Sponge symbionts also have a role in the nitrogen metabolism of their hosts, the presence of
358
nitrogen fixing bacteria in the Indo-Pacific coral reef sponge Callyspongia muricina was
359
described by (Wilkinson et al., 1999). Sponge-associated fungi have a significant role in the
360
nutrient recycling in their environment (Proksch et al., 2008; Colman, 2015). The association of
361
these fungi as obligate symbionts of these sponge species remains unclear. In a nutrient stress
362
condition, sponge associated bacteria effectively regulate nitrogenous wastes excreted from the
363
sponge host to maintain uptake of inorganic nitrogen (Fig. 3). Ammonia-oxidizing bacteria of the
364
genera Nitrosospira and Nitrosococcus (Mohamed et al., 2010) and the ammonia-oxidizing
365
archaea, such as candidatus Cenarchaeum symbiosum (Park et al., 2010) plays an important role
366
in the conversion of ammonia to nitrite in sponges. Nitrite oxidizing bacteria (NOB) such as
367
Nitrospinaand Nitrospira (Off et al., 2010; Feng et al., 2016) as well as denitrifying bacteria such
368
as Pseudovibrio denitrificans (Bondarev et al., 2013) have been identified in many sponge
369
species. In sponge associated bacteria, the assimilation of ammonia takes place through
370
glutamine synthase- glutamine oxoglutarate aminotransferase (GS-GOGAT) pathway (Fig. 2)
371
and the genes encoding for urease and urea transporters have been described (Hallam et al.,
372
2006; Siegl et al., 2011).
373
4.3. Carbon fixation
374
During the symbiotic association between sponges and microbes, the microbes use a variety of
375
sugar and carbon compounds from sponges for their nutritional benefits. Poribacteria are
376
involved in autotrophic carbon fixation which contain ATP- citrate lyase genes involved in the
377
reductive TCA cycle (Siegl et al., 2011). The sponge C. concentrica associated with
378
Deltaproteobacteria were found to have association with cyanobacteria (Hentschel et al., 2012).
379
Autotrophic carbon assimilation has been reported previously in Cenarchaeum symbiosum, a
380
crenarchaeota symbiotically associated with axinellid sponges (Hallam et al., 2006).
381
4.4. Other metabolism
382
Several species of boring sponges are found symbiotically associated with zooxanthellae and this
383
symbiotic association enhances the growth rate of the sponge via enhancing decalcification and
384
increasing boring capacity of the sponge (Hill et al., 1996). Creatine is synthesized by most of
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the invertebrates including sponges (Lavy et al., 2014), and can be converted in-vivo non-
386
enzymatically and irreversibly to creatinine by creatinase. Creatinase coding genes has been
387
found in sponge-associated bacteria from multiple sponge species, demonstrating the ability of
388
the sponge symbionts to degrade and use metabolic intermediates such as creatinine,
389
pyrimidines, or 5-oxoproline (Lavy et al., 2014).
390
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The sponge and the microbes interactby the presence of ankyrin repeat (AR) and TPR proteins
392
which mediate protein-protein interaction in eukaryotes (Fig. 2). These proteins are involved in
393
various functional processes like transcriptional initiators, cell cycle regulators, cytoskeleton
394
proteins, ion transporters and signal transducers (Thomas et al., 2010; Liu et al., 2011).The
395
putative sponge-specific bacterial family Poribacteria can produce methyl-branched fatty acids
396
(Hochmuth et al., 2010) and metabolic interactions are shared between the host Cymbastella
397
concentrica and its symbiont community (Thomas et al., 2010). There were several putative
398
host-interaction factors like Ig like domains and laminin G domain proteins which were involved
399
in adhesion and the presence of eukaryotic domains such as ankyrin, Sel1, fibronectin type III,
400
leucin-rich repeat. These proteins provide the information of host poribacterial interaction
401
(Taylor et al., 2007a; Taylor et al., 2007b)Ankryinsare important as theyare involved in the
402
recognition and protection from host phagocytosis (Liu et al., 2012).
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403
5. Dynamics of sponge microbiome
405
Bacterial phyla which have been identified from sponges include, Acidobacteria, Actinobacteria,
406
Bacteroidetes,
407
Gemmatimonadetes, Nitrospira, Planctomycetes, Proteobacteria (Alpha, Beta, Delta and
408
Gammaproteobacteria), Spirochaetes, and Verrucomicrobia (Kim, 2015). In addition to these,
409
fluorescence in situ hybridization (FISH) studies showed the presence of Rhopaloeides odorabile
410
(Webster et al., 2001). Fusobacteria have been isolated from New Zealand sponge Stellata
411
maori, and it appears to be the only phylum present in that sponge (Schmitt et al., 2012).
412
Archaea reported from marine sponges include the members of the phylum Crenarchaeota with
413
a few from the phylum Euryarchaeota (Pesaro and Widmer, 2002; Zhang et al., 2015a).The
414
group Crenarchaeotais prominent in marine environments (Polonia et al., 2014). 16S rRNA gene
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404
Cyanobacteria,
Deinococcus-Thermus,
Firmicutes,
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14
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415
library constructed from the freshwater sponge Spongilla lacustris provides sequences from the
416
Actinobacteria, Chloroflexi, and Alpha- and Beta-proteobacteria (Gernert et al., 2005).
417
Eukaryotic microbes were also reported to be present in sponges. In a recent study, sponge-
419
associated fungus, Truncatella angustata has been reported to produce Truncateols, a new
420
isoprenylated cyclohexanols with anti-H1N1 virus activities (Zhao et al., 2015). Limited
421
information is available as far as the sponge-associated viruses were concerned, while virus-like
422
particles have been observed in cell nuclei of Aplysina (Verongia) Cavernicola (Vacelet and
423
Gallissian, 1978). They may have a role to play in sponge cell pathology. In addition to the high
424
microbial diversity, more subtle patterns of host-symbiont distributions were recognized.
425
Sponges with high microbial abundance have been isolated from their different reproductive
426
stages as reported by Schmitt et al., (2008). The results from the previous studies prove the
427
unique existence of sponge-specific bacterial clusters (Schmitt et al., 2012).
428
5.1. Environmental factors
429
External environment conditions and host factors affect sponge microbial associations, but most
430
of the microbes are highly stable and resistant to physical and chemical agents. Starvation,
431
exposure to antibiotics, and even translocation of sponges such as Aplysina aerophoba (Friedrich
432
et al., 2001) and Aplysina cavernicola(Thoms et al., 2003) to different depths for brief periods
433
can cause only minor changes in their bacterial composition. Also, Aplysina fistularis which
434
wastranslocated from its natural depth of 4 m to an increased depth of 100 m showed no
435
significant changes in the cyanobacterial population (Maldonado and Young, 1998). In a recent
436
study conducted by Seo et al. (2016), bacterial profiling of three species of sponges namely,
437
Lubomirskia baicalensis, Baikalospongia intermedia and Swartschewskia papyracea by
438
pyrosequencing indicated abundance of Cyanobacteria. Diversity of the bacterial community in
439
S. papyracea was higher as compared to L. baicalensis and B. intermedia. Particularly, the
440
relative
441
2016). Thioautotrophic symbionts have been discovered from deep sea sponges like
442
Pachastrella sp. and share 99% sequence similarity with the thiosymbionts recovered from
443
poecilosclerid sponges and bathymodiolus mussels (Nishijima et al., 2010). However, elevation
444
of temperature causes a dominant shift in microbial community on marine sponges and also
445
decline in its health (Nishijima et al., 2010). A significant reduction in microbial population was
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15
abundance
of
Actinobacteria
was
higher
in
S.
papyracea
(Seo
et
al.,
ACCEPTED MANUSCRIPT
446
observed in the adult Rhopaloeides odorabilewhen the thermal threshold of 31–32ºC was slightly
447
shifted to 33ºC causing necrosis and loss of microbial symbionts (Simister et al., 2012).
448
Eutrophication causes significant changes in the diversity of the sponge-associated microbes
450
(Sabarathnam et al., 2010). It provides high influx of nutrients such as nitrogen and phosphorus,
451
which leads to increase in phytoplankton and bacterial populations which, in turn leads to a
452
higher biological oxygen demand (BOD) and increases the sedimentation rate of particulate
453
matter (Nogales et al., 2011). In contrast, Webster et al. (2014) reported that eutrophication had
454
no short-term effect on Cymbastela stipitata holobiont. (Luter et al., 2014).In earlier stages of
455
nutrient influx in Chesapeake Bay (Kan et al., 2008), bacterial communities were predominated
456
by SAR11, SAR86 and picocyanobacteria, however continued depletion of oxygen caused a shift
457
in the bacterial community to anaerobic members of the Firmicutes, Bacteroidetes and Sulphur-
458
oxidizing Gammaproteobacteria(West et al., 2016).The mechanisms of sponge microbial
459
associations are not well understood, but there were many theories that have beenproposed to
460
explain thesponge-microbial association. One of the theories suggestthat spongeduring its filter-
461
feeding selectively absorbs specific bacteria from the surrounding water containing
462
diversebacteria (Webster and Blackall, 2009). One more explanation is that there is a vertical
463
transmission of symbionts through the gametes of the sponge by inclusion of the bacteria in the
464
oocytes or larvae (Lee et al., 2009).
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465
6. Sponge-coral association: invasive or beneficial?
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Evolutionary link between sponge and coral reef has been increasing significance in
468
the functions of marine ecosystem. Sponges are playing a very important, beneficial role in
469
coral reef and ecosystem construction process, rather than destructive. Studies on the association
470
between sponge and corals are not well understood due to the difficulties in long term monitor,
471
sampling and follow-up, however, the maintaining the reef ecosystem dynamics is being obvious
472
beneficial role. Sponges are known to be facilitate corals in many ways including providing
473
nutrient (sponge loop), making suitable environment by clearing water and providing substrate
474
(stabilizing dead coral rubbles) for new recruits (Goreau and Hartman, 1963; Wulff and Buss,
475
1979; Rutzler, 2012; Rix et al., 2016a).
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477
6.1. Beneficial Food chain dynamics has important role in controlling the population and the whole
479
ecosystem dynamics (Fretwell, 1987). The dissolved organic carbon (DOC) plays a critically
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role in carbon cycle. Sponges and corals work together and transfer the dissolved organic
481
matter to higher organisms in the form of food and the process is refereed as “sponge loop”.
482
In which sponge released DOC to water column trapped by the coral released mucus and
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transferred to higher organisms (Rix et al., 2016a). This similar process confirmed through
484
laboratory isotope studies and observed in both shallow, warm water and deep sea cold water
485
corals reef system (Rix et al., 2016b). Recent study carried out at Florida Keys also supports
486
influence of sponge-derived DOM on chemical and ecological processes in coral reef ecosystems
487
(Fiore et al., 2017). Moreover, the research on sponge associated bacteria form granules evident
488
that microbes play a critical role in the phosphorus sequestration and phosphorous recycling in
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the environment (Zhang et al., 2015b). As the research efforts are being taken worldwide to
490
understand complete functional role of this relationship for better conservation of the ecosystem.
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Apart from the nutritional exchange, filter feeding mechanism of sponges in water
492
column has also been play an important role in reef health by facilitating suitable environment
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from turbid for corals to grow and reproduce. The quick recovery of reefs from turbid
494
environment caused by Hurricane was stated as best example and the studies carried out at
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hurricane affected reefs at Florida Keys revealed the correlation between sponge abundance
496
(Filtering effects) and speedy recovery (Woodley et al., 1981). In addition, Mutualistic
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association of sponge with corals also has been reported that, sponge gets space for growth
498
underneath the coral colonies, whereas the coral colony gets protected from bioeroders (Goreau
499
and Hartman, 1966; Hill, 1998). As an extra profit, exhalant water from sponge enhances the
500
food supply for corals that in turn increase coral growth, especially for coral polyps at the colony
501
edge next to the sponge (Wulff, 2012). Serious of studies carried out by Wulff (2012) clearly
502
highlighted the role that sponges can play in reef stabilization, consolidation and regeneration
503
(Wulff, 1984; 2001; 2012). The research work done by Rasser and Riegl (2002) revealed the
504
importance of sponge binding on Holocene coral reefs.
505
6.2. Invasive
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Although coral and sponges co-existed and maintain the balance in the marine
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ecosystem for a very long period, there has been a report on coral sponge interaction and few
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reports on the short term impact to the coral communities (Jackson and Buss, 1975; Vicente,
509
1978; Suchanek et al., 1983). Several research studies indicates that, there were about 95
510
sponge species and 21 coral species engaged in sponge/coral interactions with minimal damage
511
to overgrown coral colonies (Aerts, 1998). Although, the sad thing about the association is few
512
sponge invasion and competitive succession over the corals has been increase and expanded
513
its geographical locations due to climate change and the anthropogenic stress (Bell et al.,
514
2013). In particular, the sponges such as Chondrilla nucula, Cliona spp. and Terpios hoshinota
515
were aggressively grown over live corals and killed (Hill, 1998; Suchanek et al., 1983; Liao et
516
al., 2007; Thinesh et al., 2015; 2017). However, the mechanism of this sponge association over
517
corals and factors which influence the sponge outbreak is poorly been understood.
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The coral killing sponge T. hoshinota, Terpios has been expanding its geographical
519
locations and cause mortality over 30 to 80% to many coral genera (Bryan, 1973). The invaded
520
reefs collected from American Samoa and Philippines (Plucer-Rosario, 1987), Japan (Rutzler
521
and Muzik, 1993; Reimer et al., 2011b), Taiwan (Liao et al., 2007), Great Barrier Reef in
522
Australia (Fujii et al., 2011), Indonesia (De voogd et al., 2013), recently in India (Thinesh et al.,
523
2015) and Mauritius (Elliott et al., 2016b). Atpresent, the sponge Terpios is being considered as
524
a “Nuisance Species” to coral reef ecosystem. Similarly, the Cliona sp. was also recorded as
525
abundance at coral reef environment (Ruzler, 2002: Schonberg and Ortiz 2008, Ward et al.,
526
2005; Kelmo et al., 2013).
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In Belize Cliona caribbaea covered two folds between 1979 and 1998 (Ruzler, 2002).
528
In Florida Keys the increasing trend has been noticed between 1996 and 2001 (Ward et al.,
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2005). The similar trend was also recoded in Queen land reef of Australia between 1998 to
530
2004. Most of the invasive studies were done at a short period of time; hence, long term
531
assessment is the most important factor for the complete understanding of the effect. In terms
532
of understanding the mechanism for overgrowth of sponges, very few studies have been
533
attempted in Terpios. In accordance with the literature reported, the steps involved in the
534
mechanism of sponge invasion are summarized i) Dense populations of photosynthetic
535
cyanobacteria in the mesohyl could aid the sponge to enter into an active competition with
536
the corals, thereby leads to overgrowth by tendrils on the live corals (Wang et al., 2015; Elliott
537
et al.,2016a) ii) release of chemical deterrents to the ecosystem, leads the production of
538
cytotoxic compounds which weaken the coral tissue (Wang et al., 2015; Elliott et al., 2016a)
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iii) Tang et al. (2011), The changes in the microbial assemblages that accompany the invasion
540
process might weaken the coral and that resulted the sponge to attain succession during the
541
period of invasive growth. The exact ecological reason and the mechanism behind this invasive sponge outbreak
543
are remains unknown. However, the increasing evidence: Influence of ocean acidification,
544
climate change and pollution has the link to sponge outbreaks (Rutzler and Muzik, 1993;
545
Reimer et al., 2011b; Schils, 2012; Powell et al., 2014; Thinesh et al., 2017). On the hole, the
546
research studies and the long term co-existence of sponges in the healthy reef environment,
547
observed invasive impact most frequently at the sites where environmental conditions are
548
polluted and affected by climatic threats highlights the importance of sponges in the marine
549
ecosystem rather than destructive. Hence, further studies on the association particularly
550
nutritional exchange at different geographical locations with different environmental
551
conditions could provide valuable information to protect our ecosystem better.
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7. Conclusion
554
Marine sponges are sedentary aquatic animals harboring microbial symbionts upto 50% of
555
sponge biomass. Sponge-microbial association is a subject of investigation since unique
556
beneficial effects of host-symbionts remain unresolved. Albeit reports evident that sponge-
557
specific symbionts are responsible for synthesis and sequestration of sponge-derived bioactive
558
molecules, it has been reported that the sponge-microbiome consortia are not consistent in
559
different niches and geographical locations.The concept of microbiome dynamics, particularly
560
change of diverse sponge microbiome to specific abundant microbiome for the synthesis of
561
bioactive molecules, perhaps occurred as a response to external pressure such as predation or
562
competition and it should be mainstream focus of sponge microbiome research. The available
563
literature does not have any conclusive data to show the recruitment/exchange of microbial
564
symbionts between sponge and associated macroorganisms. The nutritional exchange between
565
sponge and microbial symbiont is illustrated in this review as an ecological benefit of sponge
566
microbial association. The symbiotic microbes play a significant role in the nutrient recycling of
567
sponge excreta and availability of nutrient in the surrounding seawater facilitate abundance of
568
planktonic organisms. Most of the available literature on sponge-coral association explains
569
invasive nature of sponges, but in situ shading-experiments have proven that changes in the
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microbial assemblage of sponge would reduce the colorization capacity over corals. However
571
further research is warranted on microbiome dynamics and symbiont acquisition which would
572
reveal unique symbiotic interactions.
573
Acknowledgements:
575 576 577 578
Authors are thankful to DBT, New Delhi for financial support. Authors SS & PR also thankful to University Grants Commission (UGC) for providing financial assistance in the form of Postdoctoral fellowship.
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Fig. 1. Interactions of holobionts and host sponge. Holobionts secret quorum sensing (QS)
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molecules (bioluminescence – lux, acyl homoserine lactones – AHL, rhamnolipids – RHL,
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biosurfactants etc.) for recruitment and selection of host specific holobionts and storage
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molecules like poly-hydroxy alkanoates – PHA for survival of holobionts in nutrient limited
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sponge niche. Host sponge offers shelter to the holobionts whereas holobionts secrete
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phospholipase A2 – PLA2 for synergistic host defense and bioactive molecules for host’s
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protection against pathogens, predation and fouling.
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Fig. 2. Ecological interactions and functional roles of sponge associated holobionts
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Fig. 3. Nitrogen fixation in marine sponges (Microorganisms involved have not been yet
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identified completely)
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Fig. 4. Sponge-coral association may be invasive to corals. But the functional roles and
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ecological interactions including recruitment of holobionts still remains to be explored
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Intends to describe sponge associated unique microbial symbionts An insight of eukaryotic symbionts-fungi, yeast etc., Visualization of coral killing sponge T. hoshinota, Terpios Influence of environmental factors on sponge association
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