Biodiversity of the Genus Penicillium in Different Habitats

C H A P T E R

1 Biodiversity of the Genus Penicillium in Different Habitats Ajar N. Yadav1, Priyanka Verma1, Vinod Kumar1, Punesh Sangwan1, Shashank Mishra2, Neha Panjiar2, Vijai K. Gupta3 and Anil K. Saxena4 1 3

Eternal University, Sirmour, Himachal Pradesh, India 2Birla Institute of Technology, Ranchi, Jharkhand, India ERA Chair of Green Chemistry, Tallinn University of Technology, Tallinn, Estonia 4ICAR-National Bureau of Agriculturally Important Microorganisms, Kusmaur, Uttar Pradesh, India

1.1 INTRODUCTION Penicillium is an important genus of phylum ascomycota, found in the natural environment as well as in food and drug production. Some members of the genus produce penicillin, a molecule used as an antibiotic that kills or stops the growth of certain kinds of bacteria inside the body. Other species are used in cheese making. It has a worldwide distribution and a large economic impact on human life. Its main function in nature is the decomposition of organic materials, where species cause devastating rots as pre- and postharvest pathogens on food crops (Frisvad and Samson, 2004), as well as for the production of a diverse range of mycotoxins (Frisvad and Samson, 2004). Some species also have positive impacts, with the food industry exploiting some species for the production of speciality cheeses, such as Camembert or Roquefort (Giraud et al., 2010) and fermented sausages (Lo´pez-Pe´rez et al., 2015). The degradative ability of Penicillium is due to the production of novel hydrolytic enzymes (Raper and Thom, 1949; Li et al., 2007; Adsul et al., 2007; Terrasan et al., 2010). Its biggest impact and claim to fame is the production of penicillin, which revolutionized medical approaches to treating bacterial diseases (Chain et al., 1940; Abraham et al., 1941). Many other extrolites have since been discovered that are used for a wide range of applications (Frisvad and Samson, 2004). Pitt (1979) considered it axiomatic that Penicillium or one of its products has affected every modern human. Extreme environments represent unique ecosystems that harbor novel biodiversity (Saxena et al, 2016). Penicillium is well known and one of the most common fungi found in a diverse range of habitats, including soil, air, extreme environments (temperature, salinity, water deficiency, and pH), and various food products. The genus Penicillium is ubiquitous in many environments. Since 1957, several novel species have been found such as Penicillium isariaeforme (Stolk and Meyer, 1957), Penicillium novaecaledoniae (Smith, 1965), Penicillium caerulescens (Quintanilla, 1983), Penicillium krugerii (Ramirez, 1990), Penicillium parvulum (Peterson and Horn, 2009), Penicillium buchwaldii (Frisvad et al., 2013), Penicillium corvianum (Visagie et al., 2016) from soil; Penicillium maclennaniae (Yip, 1981), Penicillium radicum (Hocking et al., 1998), and Penicillium virgatum (Kwasna and Nirenberg, 2005) from rhizospheric soil, Penicillium aurantio-flammiferum, Penicillium gallaicum, Penicillium granatense, Penicillium ilerdanum, Penicillium cordubense (Ramirez et al., 1978), Penicillium simile (Davolos et al., 2012) from air; Penicillium hispalense (Ramirez and Martı´nez, 1981), Penicillium araracuarense, Penicillium wotroi, Penicillium vanderhammenii, Penicillium penarojense, Penicillium elleniae (Houbraken et al., 2011) from phyllosphere; Penicillium nodositatum (Valla et al., 1989), Penicillium allii (Vincent and Pitt, 1989), Penicillium ellipsoideosporum (Wang and Kong, 1999), Penicillium excelsum (Taniwaki et al., 2015), Penicillium cataractum (Visagie et al., 2016), and Penicillium chroogomphum (Rong et al., 2016) from endophytic tissue of stems, roots, or seeds; Penicillium zacinthae

New and Future Developments in Microbial Biotechnology and Bioengineering. DOI: http://dx.doi.org/10.1016/B978-0-444-63501-3.00001-6

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1. BIODIVERSITY OF THE GENUS PENICILLIUM IN DIFFERENT HABITATS

(Ramirez and Martı´nez, 1981), Penicillium rubefaciens, Penicillium vaccaeorum (Quintanilla, 1982), and Penicillium jejuense (Park et al., 2015) from marine, saline soil, or mangroves; Penicillium soppii, Penicillium lanosum (Frisvad et al., 2006), Penicillium svalbardense (Sonjak et al., 2007b), Penicillium amphipolaria (Visagie et al., 2016) from cold environments; Penicillium argillaceum (Stolk et al., 1969) from hot springs; Penicillium hispanicum (Ramirez et al., 1978), Penicillium mali (Gorlenko and Novobranova, 1983), Penicillium psychrosexualis (Houbraken et al., 2010a), Penicillium viticola (Nonaka et al., 2011), Penicillium daejeonium (Sang et al., 2013) from different fruits surface; Penicillium panissanguineum, Penicillium tanzanicum (Visagie et al., 2016) from Termite mounds; Penicillium mallochii, and Penicillium guanacastense (Rivera et al., 2012) from gut caterpillars; and Penicillium costaricense (Visagie et al., 2016) from intestines of Rothschildia. The genus Penicillium is one of the most versatile “mycofactories,” comprising species able to solubilized phosphorus, produce plant growth promoting phytohormones (indole acetic acid and gibberellic acid), and produce siderophore, HCN, ammonia, and other bioactive compounds that can modulate plant growth and development (Whitelaw et al., 1997; Khan et al., 2008; Leita˜o and Enguita, 2016). The genus Penicillium may be used for bioremediation (Bhargavi and Savitha, 2014; Chan et al., 2016). The wide range of biosurfactants has been synthesized by diverse species of Penicillium, which include glycolipids, lipopeptides, phospholipids, fatty acids, and polymeric compounds. Biosurfactants and bioemulsifiers commonly have advantages such as biodegradability, low toxicity, selectivity, and biocompatibility over chemically synthesized surfactants, as well as being effective at extreme pH, temperature, and salinity. These properties enable their wide application in areas such as the bioremediation of pollutants and in the food, cosmetics, and pharmaceutical industries. The wide range of extracellular enzymes produced by the Penicillium species plays an important role in the microbiological break down of organic materials (Cha´vez et al., 2006; Gusakov and Sinitsyn, 2012).

1.2 ISOLATION AND CHARACTERIZATION OF PENICILLIUM As Penicillium is ubiquitous, it can be isolated from diverse extreme environments as well as from plants (epiphytic, endophytic, and rhizospheric) and decaying fruits. (Fig. 1.1). Penicillium from extreme environments and plants can be isolated by using different growth media such as cornmeal agar, czapek dox agar, potato dextrose agar, rose bengal agar, sabouraud dextrose agar, and vegetable juice agar (V8) (Table 1.1). Culturable Penicillium from sediment, soil, and rhizospheric soil can be isolated through enrichment using a standard serial dilution plating technique. Epiphytic Penicillium species can be isolated using ‘leaf imprinting’ methods (Verma et al., 2016a,b). Endophytic Penicillium may occur in low numbers and sometimes in localized positions within plants and thus it is almost impossible to find its specific affiliation with the host plant. For isolation of endophytic Penicillium, attention needs to be paid to avoid contamination with undesirable epiphytic microbes. It is recommended to first sterilize the entire surface of the samples, followed by cutting their organs and tissues into pieces with a sterilized knife, if necessary. Sodium hypochlorite is the most commonly used disinfectant. Plant samples usually are sterilized by sequential immersion in 70% ethanol for 1
3 minutes and 1%
3% sodium hypochlorite for 3
5 minutes, followed by repeated rinsing in sterile water to remove residual sodium hypochlorite. Hydrogen peroxide and mercuric chloride are also effective disinfectants (Suman et al., 2016). In another method, segments of the sterilized samples are placed onto an appropriate agar medium, followed by incubation at an appropriate temperature (5
45 C). Another method for isolation in which initially the samples are ground with 5 mL of aqueous solution (0.9% NaCl) using sterile mortar and pestle is also used. The tissue extract is subsequently incubated at 30 C for 3 hours to allow the complete release of endophytic microorganisms from the host tissue (Fig. 1.1). To isolate different species of Penicillium, different growth medium and condition can be used e.g. for halophilic (5%
20% NaCl concentration); drought tolerant (7%
10% polyethylene glycol); acidophilic (pH 3
5); alkaliphilic (pH 8
11); psychrophilic (incubation at .5 C temperature); thermophilic (incubation at .45 C temperature), etc. (Verma et al., 2013, 2014; Suman et al., 2015; Yadav et al., 2015d). The agar plates can be incubated for up to 1
15 days and the pure and distinct colonies can be selected according to their time of growth and morphology. The distinct Penicillium colonies can be purified by repeated inoculation on their respective growth medium plates. The pure cultures can be maintained at 4 C as slant and lyophilized. The simplified diagrammatic scheme in Fig. 1.1 shows the steps of isolation and identification of Penicillium species. The different morphotype diverse species of Penicillium are represented in Fig. 1.2.

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FIGURE 1.1 A schematic representation of the isolation, characterization, and identification of Penicillium species from different habitat.

1.3 MOLECULAR DIVERSITY AND PHYLOGENETIC ANALYSIS* More than 200 years ago, Link (1809) introduced the generic name Penicillium, meaning “brush,” and described the three species as Penicillium candidum, Penicillium glaucum, and Penicillium expansum. Since then, more than 1000 names have been introduced in the genus Penicillium. Many of these names are not recognizable today because descriptions are incomplete by today’s standards. Some names are now considered synonyms of other species. Thom et al. (1930) revised all species described until 1930 (it may be more than 1000) and accepted 300

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TABLE 1.1

Media Composition for Isolation and Biochemical Characterization of Penicillium

S. No

Media

Compositions per liter

1.

Cornmeal Agar

Cornmeal 20 g; Peptone 20 g; Dextrose-20 g; Agar 20 g

2.

Czapek Dox Agar

Sucrose 30 g; Sodium nitrate 2 g; Dipotassium phosphate 1 g; Magnesium sulfate 0.5 g; Potassium chloride 0.5 g; Ferrous sulfate 0.01; Agar 20 g

3.

Potato Dextrose Agar

Dextrose 20 g; Potato extract 4 g (200 g of potato infusion); Agar 20 g

4.

Rose Bengal Agar

Papaic digest of soyabean meal 5 g; Dextrose 10 g; Monopotassium phosphate 1 g; Magnesium sulfate 0.5 g; Rose bengal 0.05 g; Agar 20 g

5.

Sabouraud Dextrose Agar

Mycological peptone 10 g; Dextrose 40 g; Agar 20 g

6.

Vegetable Juice Agar (V-8) V-8 juice 180 mL; Calcium carbonate 2 g; Agar 20 g

FIGURE 1.2 Morphology of different Penicillium species on different growth media.

species. In later studies, Raper and Thom (1949) accepted 137 species, Pitt (1979) accepted 150 species, and Ramirez (1982) accepted 252 species. At that time, a morphological species concept was used for Penicillium classification and identification, with DNA sequencing starting to be used during the before 1990s. In fact, this became common practice as many old species were shown to be distinct and were reintroduced (Houbraken et al., 2011). The abandonment of the new International Code of Nomenclature for algae, fungi, and plants resulted in a single name nomenclature I. PENICILLIUM: BIOLOGY TO BIOTECHNOLOGY

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1.3 MOLECULAR DIVERSITY AND PHYLOGENETIC ANALYSIS

for fungi (McNeill et al., 2012). In anticipation of this change, Houbraken and Samson (2011) redefined the genera in the family Trichocomaceae based on a four-gene phylogeny. They segregated the Trichocomaceae into three families: Aspergillaceae, Thermoascaceae, and Trichocomaceae. To accommodate the morphological variation, the generic diagnosis of Penicillium was amended by Houbraken and Samson (2011). New techniques incorporated into taxonomic studies resulted in the physiological species concept (Cruickshank and Pitt, 1987) and phylogenetic species concept (Skouboe et al., 1996; Peterson, 2000), and eventually led to the combined approach using morphological, extrolite, and genetic data in a polyphasic species concept (Frisvad and Samson, 2004). Genus Penicillium may also be identified using amplification and sequencing of different genes such as β-tubulin (BenA) (Glass and Donaldson, 1995), Calmodulin (CaM) (Hoog and Ende, 1998), and RNA polymerase II, the second largest subunit (RPB2) (Liu et al., 1999). Isolates of the genus Penicillium may also be identified at the species level by comparison with ex-type cultures using morphology, physiology, and extrolite profiles (Houbraken et al., 2010b, 2014). In the following, a general methodology for molecular identification and taxonomic analysis of Penicillium species is described. Initially the Penicillium isolates should be grown in specific broth medium, until they reached in its stationary phase. The cells pellet from 5 mL culture can be washed thrice with TE buffer (10 mM Tris and 1 mM EDTA, pH 8.0) and the pellet should be resuspended in 750 μL TE buffer. Genomic DNA can be isolated from the suspended pellet using Zymo Research Fungal/Bacterial DNA MicroPrep following the standard protocol described by the manufacturer (Kumar et al., 2014b). The ITS1
5.8S
ITS2 rDNA region should be amplified using polymerase chain reaction (PCR). Reaction mixtures (25 μL) consisted of 2.5 μL 10 3 Taq polymerase Buffer A, 2.5 U Taq polymerase, 250 μM dNTPs and 0.250 μM of primers ITS1 and ITS4 (White et al., 1990). Useful primers for identification and amplification conditions for the PCR are given in Tables 1.2 and 1.3. After amplification the PCR products should be resolved by electrophoresis in 1.2% agarose gel in 1 3 TAE buffer. Gels are stained with ethidium bromide (10 mg/mL), visualized on a gel documentation system (Alpha-Imager), and the gel images are digitalized. PCR products should be sequenced using a BigDye terminator cycle sequencing premix kit and sequenced with an ABI PRISM 310 genetic analyzer. Sequence contigs should be assembled using SeqmanII (DNAstar), aligned in ClustalX. The partial transcribed spacer region (ITS) or 18S rRNA gene sequences are compared with sequences available in the NCBI database. Isolates can be identified at species level on the basis of 18S rRNA gene-sequence similarity of $ 97% with the sequences in GenBank. Sequence alignment and comparison was done using the multiple sequence alignment tool CLUSTALW2 with default parameters. The phylogenetic tree (Fig. 1.3) can be constructed on aligned data TABLE 1.2

Primers Used for Amplification and Sequencing for Penicillium Identification

Genes

Name of primer Sequences (50 -30 )

References

Internal Transcribed Spacer (ITS)

ITS1-F

White et al. (1990)

ITS4-R

TCC TCC GCT TAT TGA TAT GC

β-Tubulin (BenA)

Bt2a-F

GGT AAC CAA ATC GGT GCT GCT TTC Glass and Donaldson (1995)

Bt2b-R

ACC CTC AGT GTA GTG ACC CTT GG

CMD5-F

CCG AGT ACA AGG ARG CCT TC

CMD6-R

CCG ATR GAG GTC ATR ACG TGG

Calmodulin (CaM)

TCC GTA GGT GAA CCT GCG G

RNA polymerase II second largest subunit (RPB2) 5F-F

Hoog and Ende (1998)

Liu et al. (1999)

GAY GAY MGW GAT CAY TTY GG

7CR-R

CCC ATR GCT TGY TTR CCC AT

This table is taken from Identification and nomenclature of the genus Penicillium, Studies in Mycology, Volume 78, June 2014 by C.M. Visagie, J. Houbraken, J.C. Frisvad et al.

TABLE 1.3

PCR Amplification Programs Used for Amplification of Genes for Penicillium Identification Initial denaturing 

Cycles

Denaturing 

Annealing 

Elongation 

ITS, BenA, CaM

94 C, 5 min

35

94 C, 45 s

55 C, 45 s

72 C, 60 s

RPB2

94 C, 5 min

5

94 C, 45 s

50 C, 45 s

72 C, 60 s

5

94 C, 45 s

52 C, 45 s

72 C, 60 s

30

94 C, 45 s

55 C, 45 s

72 C, 60 s

Final elongation 

Store

72 C, 7 min

10 C, N

72 C, 7 min

10 C, N

This table is taken from Identification and nomenclature of the genus Penicillium, Studies in Mycology, Volume 78, June 2014 by C.M. Visagie, J. Houbraken, J.C. Frisvad et al.

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1. BIODIVERSITY OF THE GENUS PENICILLIUM IN DIFFERENT HABITATS

FIGURE 1.3 Phylogenetic tree of Penicillium species based on ITS1-5.8S-ITS2 gene sequences obtained from the NCBI GenBank database.

sets using the neighbor joining (NJ) method (Saitou and Nei, 1987) and the program MEGA 4.0.2 (Tamura et al., 2007).

1.4 DISTRIBUTION AND ABUNDANCE OF PENICILLIUM The genus Penicillium is ubiquitous, and can be isolated from different extreme environments (temperature, salinity, acidic, alkaline, and water-deficient habitats), associated with plants (epiphytic, endophytic, and rhizospheric), and on decaying material and different fruits. The genus Penicillium was found using both culturedependent and culture independent approaches. It is possible to assess only a small fraction of the microbial diversity from different habitats using the isolation methods described above because few microbial species can be cultivated using traditional laboratory methods. The size of microbial communities as determined using culture-independent methods might be 100- to 1000-fold larger than communities uncovered via traditional isolation (Yashiro et al., 2011). The genus Penicillium has been reported in almost every environment and plant studied. On review of different habitats and association with plants, it was found that more than 400 species of Penicillium were reported, in which seven species of Penicillium, Penicillium chrysogenum, Penicillium citrinum, Penicillium digitatum, Penicillium funiculosum, Penicillium griseofulvum, Penicillium hirsutum, and Penicillium islandicum were most predominant and reported from all types of habitats (Fig. 1.4). There are many reports on nichespecific bacterial diversity in extreme environments (Pandey et al., 2013; Kumar et al., 2014a,b; Yadav et al., 2015a,b,d; Verma et al., 2016a,b), but there are no such reports for Penicillium.

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FIGURE 1.4 Diversity and distribution of Penicillium species reported form different habitats Low temperature: Antarctica, cold deserts, Indian Himalayas, polar regions, deep sea; High temperature: Hot springs, arid regions; Saline environments: Saline soil, hypersaline region, saline lakes, marine; Fruits: Decayed fruits, apple, pomegranate, citrus, etc.; Rhizosphere: Soil, rhizospheric soil from different crops including rice, wheat, barley, chickpea, etc.; Endophytic: Endophytic microbes from different crops; Phyllosphere: Microbes from surface of different crops.

1.4.1 Low/High-Temperature Habitat There is a wide range of natural habitats where low temperatures occur continuously or intermittently due to seasonal effects. These regions include oceans, the tundra, and sub-Arctic regions. These fungi may be present either because they are true psychrophiles or because they are psychrotolerant with the ability to survive but not actively grow at temperatures ,5 C. Penicillium and different group of microbes have attracted significant attention because of interest in its cold-active enzymes and plant growth-promoting attributes at low temperatures (Yadav, 2015; Verma et al., 2015; Yadav et al., 2015a,b,c; Singh et al., 2016; Yadav et al. 2017a,b). Cold-tolerant species Penicillium have been primarily reported in connection with sub-Arctic vegetation (Babjeva and Reshetova, 1998; Fisher et al., 1995; Tosi et al., 2002), in snow and below snow-covered tundra (Babjeva and Reshetova, 1998; Schadt et al., 2003), and in permafrost (Babjeva and Reshetova, 1998; Dmitriev et al., 1997; Golubev, 1998; Tosi et al., 2002) and offshore polar waters (Broady and Weinstein, 1998). Very few studies describe their presence in Arctic glaciers. Viable fungi have, however, been isolated from Arctic and Antarctic ice, ranging in age from 10,000 and up to 140,000 years (Abyzov, 1993; Christner et al., 2000, 2003). In these cases the few isolated filamentous fungi were considered as randomly entrapped fungal Aeolian propagules originating from close and distant locations. Fungi have been only rarely isolated from glacial ice in extremely cold polar regions and were in these cases considered as random, long-term preserved Aeolian deposits. Fungal presence has thus far not been investigated in polar subglacial ice, a recently discovered extreme habitat reported to be inhabited exclusively by heterotrophic bacteria. Sonjak et al. (2006) reported on the very high occurrence (up to 9 3 103 CFU/L) and diversity of filamentous Penicillium spp. in the sediment-rich subglacial ice of three different polythermal Arctic glaciers. The dominant species was Penicillium crustosum, representing on average half of all isolated strains from all three glaciers. The other most frequently isolated species were Penicillium bialowiezense, P. chrysogenum, Penicillium commune, Penicillium discolor, Penicillium echinulatum, P. expansum, Penicillium palitans, Penicillium polonicum, Penicillium solitum, Penicillium thomii, and new Penicillium species. This was the first report on the presence of large populations of Penicillium spp. in subglacial sediment-rich ice. P. crustosum is an important and panglobal contaminant of lipid- and protein-rich foods and feeds. Although it is uncommon in extremely cold environments, we isolated a high number of P. crustosum strains from Arctic coastal areas, in particular in subglacial environments in Svalbard, Norway. P. crustosum is extremely consistent in its phenotypic properties, including morphology, physiology, and secondary metabolite production. However, some Arctic isolates differ from other Arctic and non-Arctic strains in their weak growth on creatine and in the production of the secondary metabolite and rastin A. Penicillia strains that populate glacial ice must be physiologically adaptable and able to retain their viability throughout the dynamic processes of ice melting and freezing and extremes in pressure. Such enrichment would select for Penicillium populations best adapted to dark, cold, oligotrophic environments with shifting osmotic pressures.

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Lyhne et al. (2006) reported that Penicillium jamesonlandense is a novel species from Greenland that grows exceptionally slowly at 25 C and has an optimum temperature for growth of 17
18 C. The novel species is more psychrotolerant than any other Penicillium species described to date. Isolates of this novel species produce a range of secondary metabolites with high chemical diversity, represented by kojic acid, penicillic acid, griseofulvin, pseurotin, chrysogine, tryptoquivalins, and cycloaspeptide. Penicillium ribium, another novel psychrotolerant species from the Rocky Mountains, Wyoming, in the United States, produces asperfuran, kojic acid, and cycloaspeptide. Sonjak et al. (2007a) reported that P. crustosum is a panglobally distributed foodborne fungus, extremely consistent in its morphological and physiological properties. It is also known for its consistent production of several mycotoxins and other secondary metabolites such as penitrems, roquefortines, viridicatins, and terrestric acids. It is important in temperate regions as a contaminant of oil seeds, nuts, cheese, and meat, and as producer of rot in apples. In spite of its ubiquitous nature and copious amounts of conidia it has only rarely been seen in extremely cold environments. However, in this study of mycobiota in coastal Arctic regions resulted in isolation of a high number of P. crustosum strains from different niches, such as seawater and sea ice, but primarily from the sediment-rich subglacial ice of three different polythermal Arctic glaciers. Although phenotypic properties are very homogenous in all P. crustosum isolates, some Arctic isolates differ from all other Arctic and non-Arctic strains in their weak growth on creatine, and are used as a reliable taxonomic marker and furthermore in the production of andrastin A. Sonjak et al. (2007b) isolated and characterized a novel P. svalbardense during investigation of mycobiota in coastal Arctic polythermal glaciers. Different species of the ubiquitous genus Penicillium were isolated from the extreme subglacial environment. A group of Penicillium strains was obtained that did not belong to any known Penicillium species. This species was isolated in high numbers from the Kongsvegen subglacial ice and was not detected in the surrounding environment. Detailed analysis of secondary metabolite profiles, physiological and morphological characteristics, and partial β-tubulin gene sequences showed that the proposed new species P. svalbardense is closely related but not identical to Penicillium piscarium and Penicillium simplicissimum. It differs in the production of secondary metabolites and in the morphological features of conidia and penicilli and is therefore considered as a new species. Dhakar et al. (2014) isolated and identified 25 Penicillium species from the Indian Himalayan region. Based on the phenotypic characters (colony morphology and microscopy), all the isolates were designated to the genus Penicillium. Exposure to low temperatures resulted in enhanced sporulation in 23 isolates, while it ceased in 2 isolates. The fungal isolates produced watery exudates in varying amounts that in many cases increased at low temperature. All the isolates could grow between 4 C and 37 C (optimum 24 C) and hence were considered psychrotolerant. While all the isolates could tolerate pH from 2 to 14 (optimum 5
9), 7 isolates tolerated pH 1.5 as well. While all the fungal isolates tolerated salt concentration above 10%, 10 isolates showed tolerance above 20%. Based on ITS region (ITS1-5.8S-ITS2) analysis the fungal isolates belonged to 25 different species of Penicillium. Characteristics such as tolerance for low temperature, wide range of pH, high salt concentration, and enhancement in sporulation and production of secondary metabolites such as watery exudates at low temperature can be attributed to the ecological resilience possessed by these fungi for survival in the low-temperature environments of mountain ecosystems. Barsainya et al. (2016) isolated salt-tolerant and chromium-resistant fungal strains from Pangong Lake in Ladakh. They analyzed the interaction of Penicillium spp. with chromium and NaCl and reported on the ability of Penicillium spp. to bind with chromium and NaCl in aqueous solution. It was demonstrated that NaCl reduced the extent of Cr biosorption and promoted the fungal strains of Penicillium for better growth. These findings suggest that NaCl might reduce the toxicity of hexavalent chromium in Penicillium spp. and may be used as a potential organism for remediation of chromium in high salinity environments. The genus Penicillium has the ability to grow over a wide range of temperature conditions. Fungi and microorganisms generally have been classified as thermotolerant and as true thermophiles. A thermophilic fungus is defined as one that has minimum growth at 20 C or above and a maximum growth at 50 C or above. Optima for thermophilic fungi thus occur in the range 40
50 C. Many species of Penicillium have been reported from high-temperature, arid regions such as P. chrysogenum, P. citrinum, P. digitatum, P. funiculosum, P. griseofulvum, P. hirsutum, P. islandicum, Penicillium italicum, Penicillium implicatum, Penicillium oxalicum, Penicillium georgiense, Penicillium janczewskii, and Penicillium flavigenum (Fig. 1.4). Porritt and Lidster (1978) showed that prestorage exposure of apple fruit to 38 C for 4 days suppressed both softening and naturally occurring decay, mostly due to Penicillium spp. after prolonged storage. Sams et al. (1993) reported that heating “Golden Delicious” apples for 4 days at 38 C and then infiltrating them with

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calcium-reduced decay caused by P. expansum by 30% and maintained fruit firmness during 6 months storage at 0 C. The response of apples to heat treatment may vary according to cultivar, as “Golden Delicious” and “Delicious” showed relatively strong heat tolerance (Kim et al., 1993).

1.4.2 Saline Habitat Marine microorganisms, especially marine fungi, have become one of the richest sources of structurally novel and biologically active metabolites in the marine environment. Among them, fungi derived from the deep sea have recently attracted great interest as a promising target for the discovery of pharmaceutically important metabolites due to their extreme environment. To maximize the chemical diversity available from microorganisms, new sources of microbes are needed. Deep-sea hydrothermal vents are only beginning to be investigated for bioactive natural products. Because physical and chemical conditions at deep-sea hydrothermal vent sites are highly varied and conditions are constantly fluctuating, vent sites may represent a nearly inexhaustible source of genomic innovation (Sogin et al., 2006). Many species of Penicillium have been reported from saline habitats (e.g., saline soil, hypersaline regions, saline lakes, etc.) such as P. chrysogenum, P. citrinum, P. digitatum, P. funiculosum, P. griseofulvum, P. hirsutum, P. islandicum, P. italicum, P. glaucum, P. solitum, P. georgiense, Penicillium adametzii, Penicillium bilaiae, Penicillium antarcticum, Penicillium adametzioides, and Penicillium giganteum (Fig. 1.4). Penicillium species have been isolated as endosymbionts in different seaweeds (Zuccaro et al., 2008). Gao et al. (2010) reported that P. chrysogenum QEN-24S, an endophytic fungus isolated from an unidentified marine red algal species of the genus Laurencia, displayed inhibitory activity against the growth of pathogen Alternaria brassicae in dual-culture test. Li et al. (2011) reported that Penicillium paneum SD-44 from a deep-sea sediment sample that was collected from the South China Sea displayed cytotoxicity in a preliminary bioassay. The marinederived fungi, especially the Penicillium spp., are rich sources of chemically diverse natural products with a broad range of biological activities. Among the filamentous fungi with the highest frequencies different species of the genera Penicillium from salterns and salt lakes worldwide have been isolated (Butinar et al., 2011). Although many species in the subgenus Penicillium grow well in salted foods, only five species have been recognized as part of the indigenous fungal communities. P. chrysogenum is a common, widely distributed species that appears regularly in saline lakes and salterns worldwide, while Penicillium brevicompactum is particularly common in Adriatic salterns. The other three species, two of which are most likely new, are seen consistently at low counts or at low salinities, or appear in hypersaline waters only sporadically. Penicillium sizovae and Penicillium westlingii have also been identified as part of the hypersaline mycobiota, their counts decrease with increased salinity and are considered as temporal inhabitants (Butinar et al., 2011). Leita˜o and Enguita (2016) reported a gibberellins-producing halophilic endophytic Penicillium. Although plants have the ability to synthesize gibberellins, their levels are lower when under salinity stress. It has been recognized that detrimental abiotic conditions, such as saline stress, have negative effects on plants, since the availability of bioactive gibberellins is a critical factor for their growth in these conditions.

1.4.3 Acidic/Alkaline Habitat Most fungi living in acidic habitats should be regarded as acid-tolerant rather than strictly acidophilic because they are also able to grow under neutral or even alkaline pH. Acidic natural environments with pH ranges from 3 to 4 are relatively common and include soils, lakes, swamps, and peat bogs. The fungal communities in acidic soils have been studied extensively. Acid-tolerant yeasts have been reported mainly from sandy soils (Alvarez and Vogel, 1991). Most Penicillium species prefer low pH and P. chrysogenum, P. citrinum, P. digitatum, P. funiculosum, P. griseofulvum, P. hirsutum, P. islandicum, P. italicum, P. implicatum, Penicillium roqueforti, P. oxalicum, and P. flavigenum have been reported in acidic soil (Fig. 1.4). Penicillium cyclopium acidifies the growth medium by excreting acids (mainly citric) and protons (in exchange for NH). Similar to other acidophilic microorganisms, the cells keep the average intracellular pH approximately neutral as long as the external pH stays above a certain critical value. P. oxalicum strain GZ-2 was isolated from decaying wood and produced acidophilic xylanase, which is of interest since relatively few such xylanases have been studied (Driss et al., 2011). The xylanolytic enzymes produced by P. oxalicum GZ-2 have potential industrial and agricultural applications. Extreme acidic environments, with pH values , 3, are found in many parts of the world and are of both natural and anthropogenic origin. Natural acidic habitats with pH ranges from 1 to 3 are mainly solfatara soils and have been studied in the United States, Japan, Russia, Italy, Iceland, and New Zealand. The biological

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communities of anthropogenic acidic environments such as mining effluents, coal tips, drainage water, and industrial waste water have received increasing attention in the last few decades. A large number of prokaryotic microorganisms, especially archaebacteria, have been studied for biotechnological reasons. Applications include microbial desulphurization of coal, treatment of toxic industrial wastes, and bioaccumulation of metals (Rawlings, 2013). Among eukaryotic organisms, acidophilic algae and protozoans have received more attention than fungi and yeasts (Nixdorf et al., 1998), although fungi have long been recognized as active participants in the acidification of sulfide-rich environments (Armstrong, 1921). They have also been reported in acid wastewaters (Stokes and Lindsay, 1979; Ehrlich, 1996) and underground mines where timbers are used to maintain structural integrity (Robbins et al., 1999).

1.4.4 Penicillium Associated With Plants and Fruits The genus Penicillium is ubiquitous, and has been reported from plants as phyllospheric, rhizospheric and endophytic, and from different decaying fruits. The microbial communities of leaves are represented by a variety of bacteria and filamentous fungi. The habitat adjacent to leaves is called phyllosphere and the inhabitants are called epiphytes. The environment in direct association with leaves is called phylloplane. The structure of microbial phyllosphere communities is influenced by numerous environmental parameters including UV radiation, air pollution, relative humidity, nutrients, and temperature. The phyllosphere is an open system and microbes can invade plant leaves by migration from the atmosphere, soil, other plants, insects, and animals. The microbial populations from the aerial parts of plants (phyllosphere) are involved in functional processes as large in scale as the carbon cycle, nitrogen fixation, and degradation of organic pollutants, pesticide residues. Filamentous fungi are considered transient inhabitants of leaf surfaces, predominantly as spores. Phyllosphere fungi include endophytes and epiphytes that colonize the interior and surface of the phyllosphere, respectively, occupying two distinct habitats in the leaves. Penicillium has been reported from different crops as epiphytic (Abdel-Hafez, 1981; ElSaid, 2001; Bhuyan et al., 2013; Grbi´c et al., 2015; Waing et al., 2015). The genus Penicillium has been reported from the phyllosphere of different plants such as wheat (Uddin and Chakraverty, 1996), banana (El-Said, 2001), giant dogwood (Osono and Mori, 2004), rice (Mwajita et al., 2013), Persea bombycina (Bhuyan et al., 2013), Nepeta rtanjensis (Grbi´c et al., 2015), and orchid tree (Waing et al., 2015; Fig. 1.4). El-Said (2001) isolated phyllosphere and phylloplane fungi of banana cultivated in Egypt. The 73 species and 5 varieties belonging to 36 genera were reported from the leaf surfaces of banana plants on different growth medium. Among the isolated fungi different species of Penicillium were reported such as Penicillium albdium, Penicillium chrysogemum, Penicillium citrimum, Penicillium corylophilum, Penicillium duclauxi, P. funiculosum, and Penicillium puberulum. Bhuyan et al. (2013) isolated and characterized Penicillium from plant Persea bombycina leaves. Phyllosphere microorganisms influence the growth of their host plants, either negatively as pathogens or positively by increasing the stress tolerance and disease resistance. Based on colony morphology, mycelium, sporangiophore, and spore morphology, the identified Penicillium species were dominant among all the fungal isolates. Grbi´c et al. (2015) reported Penicillium associated with phyllosphere of endemic Serbian plant Nepeta rtanjensis (Lamiaceae), an endemic and critically endangered plant species that grows only on Rtanj Mountain in southeastern Serbia. Fungi were isolated from the leaf surface and interior, and a total of 49 taxa of microfungi were identified, belonging to 35 genera. The genus Penicillium from N. rtanjensis phyllosphere are not specific to the host plant, but rather common and ubiquitous phyllosphere colonizers. According to Waing et al. (2015) Penicillium and other fungi are essential parts of the ecosystem and play an important role in the decomposition of organic material such as plant residues. It may feed on dead organic matter and return the nutrients back into the soil. Different species of Penicillium such as P. chrysogenum, P. citrinum, P. decumbens, P. hirsutum, P. implicatum, P. olsonii, P. oxalicum, and P. purpurogenum have been isolated and identified in the leaf litters of three species of forest trees; namely, rain tree (Samanea), orchid tree (Clitorea), and paper tree (Gmelina). These fungal species could be potentially used to quicken the decomposition of enormous leaf litters of forest trees. Endophytic Penicillium spp., found in the inner tissues of living plants, has attracted increasing attention among ecologists, taxonomists, chemists, and agronomists. They are ubiquitously associated with almost all plants studied to date (Wang and Dai, 2011; Suman et al., 2016). Numerous studies have indicated that these Penicillium species have an impressive array of biotechnological potential, such as enzyme production, biocontrol agents, plant growth-promoting agents, bioremediation, biodegradation, biotransformation, biosynthesis, and nutrient cycling (Strobel et al., 2004; Carvalho et al., 2012; Suman et al., 2016). These fungi may represent an

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underexplored reservoir of novel biological resources for exploitation in pharmaceuticals, industry, and agriculture. Recent studies have revealed a large richness of endophytic fungal species and diverse metabolites with different functions (Zimmerman and Vitousek, 2012; Xiao et al., 2014). In some cases, they can enhance plant growth (Waller et al., 2005), act as biological control agents (Zhang et al., 2014), and produce enzymes (Bezerra et al., 2012). The endophytic fungi are relatively unexplored and could be potential sources of novel natural products for exploitation in medicine, agriculture, and industry (Strobel et al., 2004). The different species of Penicillium have been isolated and reported as endophytic from different plants, e.g., wheat (Larran et al., 2002), Melia azedarach (Marinho et al., 2005), coffee plant (Peterson et al., 2005), rice (Naik et al., 2009), Hevea brasiliensis (Gazis and Chaverri, 2010), Ledum palustre (Tejesvi et al., 2011), Tinospora sinensis (Mishra et al., 2012), Centella asiatica (Devi and Prabakaran, 2014), Brassica napus (Zhang et al., 2014), Pinus wallichiana (Qadri et al., 2014), Solanum lycopersicum (Khan et al., 2015), Artemisia annua (Zheng et al., 2016), and Calophyllum apetalum (Chandrappa et al., 2016). The species of Penicillium are frequently encountered as postharvest contaminants of agricultural products. They can contaminate fruits and vegetables at different stages including harvest, processing, and handling. The most important aspect of food spoilage caused by these organisms is, however, the formation of mycotoxins, which may have harmful effects on human and animal health. Several mycotoxins have been identified that may contaminate foods including fruits and vegetables, the economically most important of which are aflatoxins, ochratoxins, and patulins. Different species of Penicillium have been isolated and reported from decaying fruits and vegetable and agricultural waste, e.g., apples (Frisvad and Samson, 2004; Amiri and Bompeix, 2005; Baert et al., 2007; Morales et al., 2010; Xiao et al., 2016), citrus (Snowdon, 1990; Frisvad and Samson, 2004; Holmes and Eckert, 1999; Macarisin et al., 2007; Lo´pez-Pe´rez et al., 2015), grapes (Dijksterhuis and Samson, 2007; Lorenzini et al., 2016; Ahmed et al., 2015), peanuts (Frisvad and Samson, 2004), and pineapples (Frisvad and Samson, 2004; Snowdon, 1990; Fig. 1.4).

1.5 CONCLUSION AND FUTURE PROSPECTS The genus Penicillium have been reported from different habitats including extreme environments, in plants as well as from postharvested decaying fruits and vegetables. The Penicillium isolated from extreme environments can be used to understand adaptive processes that allow life in these types of environments. The evidence of its existence in diverse habitats has consequences in exploring promising biotechnological and industrial applications. Penicillium spp. in extreme and specific environments should be studied to determine specific environmental conditions and to understand specific metabolite, enzyme, or bioactive compound production as well as applications under similar conditions. Understanding the evolution of microbes in extreme environments will increase our basic knowledge of evolutionary processes and allow better evaluation of the potential ecological consequences of environmental changes and human health. Comprehensive analysis of the diversity of Penicillium species in extreme environments has already helped in the development of a huge database that includes baseline information on the distribution of Penicillium in different niches and identifies niche specific microbes. The cultures tolerant to low and high temperature, salinity, acidic pH, and water stress represent a rich bioresource for useful genes and alleles, which can aid in the generation of abiotic stress-tolerant transgenics. Although several studies on fungal diversity are available, targeted analysis of Penicillium diversity may reveal new findings and mechanisms related to its role in nutrient recycling, environmental management, plant-growth promotion, and evolutionary processes.

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Notes *This chapter includes content (section 1.3 Molecular diversity and phylogenetic analysis, 1st paragraph) previously published in Identification and nomenclature of the genus Penicillium, Studies in Mycology, Volume 78, June 2014 by C.M. Visagie, J. Houbraken, J.C. Frisvad et al. The authors of this chapter thank and acknowledge the original authors of this work.

I. PENICILLIUM: BIOLOGY TO BIOTECHNOLOGY