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The industrial ecology of freshwater macroalgae for biomass applications
ALGAL-00673; No of Pages 6 Algal Research xxx (2016) xxx–xxx
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The industrial ecology of freshwater macroalgae for biomass applications Rebecca J. Lawton ⁎, Andrew J. Cole, David A. Roberts, Nicholas A. Paul, Rocky de Nys MACRO — the Centre for Macroalgal Resources and Biotechnology, James Cook University, Queensland 4811, Australia
a r t i c l e
i n f o
Article history: Received 1 December 2015 Received in revised form 24 August 2016 Accepted 30 August 2016 Available online xxxx Keywords: Oedogonium Bioremediation Biochar Bioenergy Wastewater Protein
a b s t r a c t Industrial ecology is focused on recognising the inherent value in waste streams and developing techniques that can efficiently recover this value. Freshwater macroalgae can become a foundation of this concept as they can be cultured in a range of waste streams where they can effectively remove excess nutrients, metals and metalloids, providing both a bioremediation service and a biomass resource. The cultured algal biomass can then be used as a product in animal feeds, biochar, biosorbents or as a feedstock biomass for the production of bioenergy. Freshwater macroalgae provide a unique opportunity to transform a range of industries through the utilisation of wastewater to produce biomass that can be converted into valuable bioproducts. © 2016 Published by Elsevier B.V.
1. Introduction
2. Large-scale cultivation of freshwater macroalgae in wastewater
Industrial ecology examines materials and energy flows in products, processes, industries and economies [1,2]. It aims to replicate the efficiencies seen in natural ecosystems and change industrial processes from linear systems, in which resources move through the system in a single direction to produce products and waste products, to systems where wastes are recycled to become inputs for new processes [1,3]. A central focus of industrial ecology is the development of processes and practices that reduce environmental impacts through the beneficial use of waste products as raw material [3] and is an innovative model for economic growth, social development and environmental management [4]. An innovative and developing industrial ecology model is to cultivate macroalgae in wastewater as a bioremediation technology, with the biomass then serving as an input for algal-based end-products such as food, feed, and bioenergy (e.g., [4]). Freshwater macroalgae provide a particularly innovative opportunity across multiple industries due to their ability to grow in a range of wastewaters and the suitability of resultant biomass for a variety of applications (Fig. 1). Our objective is to highlight and review recent research describing the large-scale cultivation of freshwater macroalgae in wastewater and their bioremediation capabilities, and provide an overview of the products which freshwater macroalgae can provide as a by-product of bioremediation. Finally, we demonstrate how freshwater macroalgae can be integrated into an industrial ecology system.
Large-scale cultivation of macroalgae in wastewater has predominantly occurred in algal turf scrubber (ATS) systems or open ponds at the scale of more than 20 kL day−1 (Table 1). ATS systems consist of an attached algal community, containing many species of macro- and microalgae and associated microbes and micro-invertebrates, which grows as a turf on screens in a shallow trough through which water is pumped [6]. The most widely used open pond system for large-scale macroalgal cultivation is the High Rate Algal Pond (HRAP) [4,7]. HRAPs are shallow, circular raceways around which water is gently circulated by a paddlewheel, maintaining the macroalgae in constant suspension. In contrast to ATS systems, which have a mixed algal community that is largely self-seeded and uncontrolled (e.g., [8]), HRAPs maintain a monoculture of a single species of macroalgae. This provides the advantage of delivering a consistent composition and source of biomass for bioproducts. Therefore, considerable research effort has focused on the identification of species of freshwater macroalgae for cultivation in outdoor pond systems. The macroalgal genera Rhizoclonium, Cladophora and Oedogonium have commonly been used for bioremediation [8–10]. However, it is clear that the cosmopolitan freshwater macroalgal genus Oedogonium has advantages in open pond systems as it is robust and competitively dominant with a biochemical composition which aligns itself well with a range of biomass applications ([11], Table 2). Oedogonium is an ideal candidate for use in an industrial ecology framework as it has high biomass productivities comparable to those of microalgae (~20 g dry weight (DW) m−2 day− 1) when cultured in a variety of water sources (Table 2), including agricultural and municipal wastewaters rich in nitrogen and phosphorus [9,12,13], and industrial wastewater
⁎ Corresponding author. E-mail address: [email protected] (R.J. Lawton).
http://dx.doi.org/10.1016/j.algal.2016.08.019 2211-9264/© 2016 Published by Elsevier B.V.
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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Fig. 1. Conceptual model of freshwater macroalgae integration in an industrial ecology system.
contaminated with heavy metals [14–17]. Additionally, it has broad environmental tolerances to temperature, nutrient concentration, salinity and water flow rate (Table 2), making it particularly suited to industrial scale cultivation where it can adapt to suit the local conditions without requiring industries to change operational protocols. There are many benefits to cultivating freshwater macroalgae in wastewater. A primary benefit is that macroalgae can be produced without using large volumes of quality freshwater, thereby reducing competition between algal production and conventional agricultural production [18,19]. Moreover, when cultivated in nutrient-rich wastewater, for example from agriculture production or municipal water treatment, freshwater macroalgae do not require any additional fertiliser inputs [10,12,20,21] reducing input costs. Cultivation of freshwater macroalgae in wastewater can provide an alternative treatment service, removing nutrients, metals and other contaminants from the wastewater (see Section 3). This also recovers nutrients or minerals in the wastewater that would otherwise be lost by using macroalgal biomass grown in wastewater as a biomass resource (see Section 4). However, there are also considerations in cultivating freshwater macroalgae in wastewater. Macroalgal biomass cultivated in wastewater contaminated with heavy metals or other toxins may be unsuitable for some biomass applications such as human and animal food, or agricultural fertiliser [23]. Similarly, if the composition of wastewater varies considerably over time, then the biochemical composition of freshwater macroalgae cultivated in this water can vary, making it unsuitable for
use in end product applications requiring algal biomass with a consistent biochemical composition. More generally the benefits and disadvantages of large scale algal cultivation of macroalgae require careful consideration, however, cultivation in wastewater alleviates some of the generic issues that have been raised in the broad scale production of microalgae, specifically contamination and harvesting [24]. 3. Bioremediation Freshwater macroalgae are highly successful at sequestering nutrients, metals and metalloids from wastewaters and in all cases the success of bioremediation is directly correlated to productivity, with increases in the growth of algae (productivity) resulting in increases in the bioremediation of contaminants [9,10,12,13,17,25,26]. As an example, for nutrient rich wastewater from agricultural production, a mixed algal species ATS system treating dairy manure had uptake rates of 0.40– 1.26 g m−2 day−1 for nitrogen and 0.06–0.22 g m−2 day−1 for phosphorus across a range of productivities from 2.5–24 g DW m−2 day−1 [10]. When cultured on-site in wastewater from an intensive freshwater fish farm, Oedogonium had comparable uptake rates of up to 0.45– 1.09 g m−2 day−1 for nitrogen and 0.08–0.13 g m−2 day−1 for phosphorus across a range of productivities from 3.8–23.8 g DW m−2 day−1 [12]. Similarly, when cultured in primary treated effluent from a municipal wastewater treatment facility, Oedogonium had stable uptake rates of up to 0.50 g m−2 day−1 for nitrogen and 0.11 g m−2 day−1 for
Table 1 Large scale cultivation of macroalgae in wastewater in Algal Turf Scrubber (ATS) systems and High Rate Algal Ponds (HRAP). System sizes are reported as length × width (m). Volume of water treated (volume) is reported as kL day−1; only systems treating N20 kL water per day have been included. FW: freshwater. Reference
Wastewater type
Type of algae used
System type
System size
Volume
[53] [10] [54] [52] [55] [51] [8] [56] [7]
Municipal, point source Dairy manure, point source Municipal, point source Municipal, point source Agriculture, non-point source Agriculture, non-point source Agriculture, non-point source Municipal, point source Aquaculture, point source
FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macroalgae Marine macroalgae
ATS ATS ATS ATS ATS ATS ATS HRAP HRAP
152 × 6.7 30 × 1 90 × 0.3 90 × 0.3 15.2 & 24.4 × 0.6 50 × 1 234 × 1.2 22 × 11 10 × 1
436–889 134 109 112–1080 55 137 327 36 36
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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Table 2 Minimum and maximum reported values for environmental conditions that Oedogonium has been cultivated under, and biochemical characteristics of Oedogonium biomass. All studies which listed specific values for each parameter are noted in the References column. Minimum
Maximum
References
Cultivation conditions Temperature (°C) Water flow rate (volumes day−1) Light (mol photons m−2 day−1) Dissolved inorganic nitrogen (DIN) concentration (mg L−1) Reactive phosphorus concentration (mg L−1) Salinity (‰)
5.8 0 (batch culture) 4.3 0.66 0.2 0
32.1 5.0 60.4 23.1 4.1 3.0
[9,11,12,14–16,42,57,58] [9,11,12,14–17,35,36,39,41,42,57,58] [9,11–16,42,57,58] [9,11–13,16,41,57,58] [9,11–13,16,41,57,58] [58,59]
Biomass characteristics Biomass productivity (g DW m−2 day−1) Total protein (wt%) Essential amino acids (% total amino acid) Total lipids (wt%) Ash (wt%) Carbohydrates (wt%) Higher heating value (MJ kg−1)
1.9 4.0 43.1 7.9 2.9 41.0 15.8
40.0 34.0 43.7 9.4 43.7 41.0 20.1
[9,11–17,41,42,58] [9,12,39,40,58] [9,58] [39,58] [9,11,13,39,41,42,47,58,60] [39,58] [11,12,39–42,48,58]
phosphorus across a range of productivities from 6.8–9.9 g DW m−2 day−1 [13]. Notably, when cultured on-site in industrial wastewaters in open ponds, monocultures of Oedogonium had metal sequestration rates of 1 mg for every g of algal productivity (g DW m−2 day−1) and this uptake rate was consistent across a range of productivities, from 2.9– 10 g m−2 day−1 [17]. Oedogonium monocultures significantly improved water quality with the continuous production and harvest of biomass from ash water reducing the concentration of Al, As, Cd, Ni and Zn in this water from initial levels in excess of water quality criteria to levels meeting guidelines within 3–28 days [16,17]. 4. Products 4.1. Animal feed Freshwater macroalgae cultured in nutrient rich (N + P) wastewater from aquaculture or agricultural production provides a high quality source of protein and trace minerals, making this biomass an attractive alternative animal feed source/supplement. The protein content of freshwater macroalgae varies among species and with cultivation conditions, however, is comparable to terrestrial crops. For example, the crude protein content in biomass comprised of multiple species of freshwater macroalgae cultivated in dairy manure ranged from 31 to 44% DW (calcuated as N × 6.25, [21]), while the crude protein content in Oedogonium biomass cultivated in aquaculture wastewater ranged from 26 to 28% DW (calcuated using a species specific conversion factor of N × 4.7, [11]). The protein in Oedogonium is particularly attractive as just under half is composed of essential amino acids, with high concentrations of methionine and lysine. Moreover, the protein content of Oedogonium can be recovered rapidly following nutrient depletion if a pulse of nitrogen is applied [27]. Freshwater macroalgal biomass also contains a range of trace elements and minerals including Ca, K, P and Mg [8– 10], which are important for animal growth and development [28,29]. Compared to decorticated cottonseed meal (DCM), a valued protein supplement used in animal feed, freshwater macroalgae have a lower crude protein content and essential amino content, a comparable gross energy content, a higher total lipid content, a lower phosphorus content and a much higher sulfur content [30]. Notably, the properties of freshwater macroalgae biomass, in particular mineral, protein and lipid content, can be manipulated by varying cultivation conditions and post-harvest processing practices [9,31], providing a mechanism to tailor biomass to the specific nutritional requirements of different animals. 4.2. Soil ameliorants Freshwater macroalgae can be converted into soil ameliorants as slow-release fertilisers or carbon-rich biochar. Freshwater macroalgae
cultivated in wastewater from animal production is an effective slow release fertiliser when applied as untreated dried and milled biomass, with equivalent effects on plant mass and nutrient content to commercial fertiliser [32,33]. Biochar, the product of the combustion of algal biomass under oxygen-limiting conditions [34], produced from Oedogonium biomass improves the retention of nutrients from fertiliser (N, P, Ca, Mg, K and Mo) in low quality soils and enhances plant growth and nutrient uptake [23]. For example, radishes grown in low quality, sandy loam soils concurrently provided with fertiliser and biochar had 35–40% higher growth rates and much higher concentrations (10– 50%) of essential trace elements (Ca, Mg, K and Mo) and macro nutrients (P) compared to radishes grown with fertiliser but without biochar [23]. Importantly, the production of biochar through slow pyrolysis provides an opportunity to utilise biomass cultured in industrial wastewater as the pyrolysis process immobilises metals accumulated by live macroalgae in the resulting biochar with lower leachable concentrations of metals compared to the biomass [17,23]. 4.3. Biosorbents Biochar produced from freshwater macroalgae can also be used as a biosorbent that effectively binds metals [35,36]. Alternatively, the biomass can be treated with an iron (Fe) solution prior to conversion to biochar to produce a biosorbent that effectively binds metalloids [35– 37]. The sequential application of biochar and Fe-treated biochar can then be used to comprehensively remove metals and metalloids from a range of industrial wastewaters [36]. This provides a specific innovation in closing the loop for industrial wastewaters where macroalgae first provide a bioremediation service through the sequestration of metals and trace elements as they grow, and secondly through further re-use as biochar to continue the treatment process. Finally, this metal and trace element rich resource can be re-used, with consideration, in the remediation of stockpiled mine soils [38]. 4.4. Bioenergy Freshwater macroalgae cultured in any type of wastewater can be used as a bioenergy resource. Higher heating values (HHV, a measure of the amount of stored energy) for freshwater macroalgae biomass range from 12.1 MJ kg−1 for Pithophora to 22.3 MJ kg−1 for Spirogyra [11,39–42]. These values are comparable to those of the alternative bioenergy feedstocks of terrestrial crop residues (11–28 MJ kg− 1), wood (12 MJ kg−1) and the industrial biomass crop Miscanthus (18.5 MJ kg−1) [41,43]. Freshwater macroalgal biomass has been successfully converted to a range of biofuels with a focus on thermochemical processes to maximise the energy yield [44]. Oedogonium and Cladophora have high yields of biocrude (27% DW and 26.3% DW
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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respectively) with high energy potential (HHV of 33.7 and 33.5 MJ kg−1 respectively) when processed using hydrothermal liquefaction [13,39]. Furthermore, the quality of the biocrude can be improved through selective post-harvest processing to reduce the quantities of heteroatoms (N + S) [31]. Cladophora and Oedogonium have been also been converted to biogas and bio-oil through slow and fast pyrolysis [40]. In alternative pathways to produce liquid fuels, Oedogonium has been used as a research scale feedstock for the production of biodiesel through the transesterification of extracted lipids [45]. However, freshwater macroalgae have a low lipid content making this process less applied at scale. In contrast, there is significant interest in the conversion of macroalgal biomass to ethanol, particularly given the biochemical composition of carbohydrates in green algae (chlorophyta), the predominant taxonomic grouping of freshwater macroalgae. For example, Spirogyra has been converted to bioethanol through fermentation [46]. Freshwater macroalgae biomass can be used as a combustible fuel [47]
and is also suitable for co-combustion with coal [48,49]. Freshwater macroalgae can also be converted to energy using biological processing through anaerobic digestion to methane and subsequent conversion to energy, most commonly through combustion. The anaerobic digestion of Rhizoclonium biomass produced 93–145 mL methane g DW−1, depending on pre-treatment methods [50]. This also provides the opportunity to deliver the closed loop re-capture of nitrogen and phosphorous as these are concentrated end-products in the wastewater from the anaerobic digestion process that are often an issue in terms of disposal. 5. Integration of freshwater macroalgae into industrial ecology systems Freshwater macroalgae provide a unique opportunity to transform a range of industries through the utilisation of wastewater streams to
A) Integrated agricultural production system
Agriculture
Waste water
Macroalgal cultivation
Feed mill
Animal production
Fertiliser
Crop production
Water re-use Clean water
Discharge
B) Integrated municipal waste production system
Municipal waste
Waste water
Macroalgal cultivation Biocrude
Refinery
Fertiliser
Crop production
Biofuel
Water re-use Clean water
Discharge
C) Integrated industrial production system
Industry Flue gas
Macroalgal cultivation Biochar
Waste water
Biocrude
Fertiliser
Refinery
Crop production
Biofuel
Water re-use Clean water
Discharge
Fig. 2. Conceptual model of integrated freshwater macroalgae production in A) agricultural systems, B) municipal waste systems and C) industrial systems.
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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produce algal biomass that can be converted into valuable bioproducts. In agricultural systems, freshwater macroalgae can be cultivated on-site in nutrient rich wastewaters, resulting in an improvement to water quality and an accumulation of N, P and other minerals and trace elements in their biomass (Fig. 2A) [8,9,12,51]. This biomass can then be used as a high quality feed ingredient or slow release fertiliser, and the treated water from macroalgal cultures could be recycled back for re-use in animal production or industrial use. In municipal waste treatment systems, freshwater macroalgae can be cultivated on-site in nutrient rich wastewaters, reducing concentrations of dissolved nitrogen and phosphorus in the wastewater (Fig. 2B) [13]. The resultant biomass can then be converted into a range of bioenergy resources such as biocrude, biogas, bio-oil or ethanol [13,39–41] and the treated water from macroalgal cultures could be recycled back for re-use in municipal waste treatment or safely released to the environment. The biomass could also be converted to biochar and used as a soil ameliorant [23]. In industrial systems, freshwater macroalgae can be cultivated on-site in waste effluents, removing contaminants and treating water (Fig. 2C) [13,14,17,52]. The resultant biomass can then be dried or converted to biochar and used as a biosorbent to further treat these metal-rich wastewaters [35,36]. The biochar can also be used as an ameliorant for low-fertility soils, for example to aid in mine site rehabilitation [23]. Alternatively, the resultant biomass can be converted into a range of bioenergy resources such as biocrude [39–41]. Finally, treated water from macroalgal cultures can be recycled back for re-use in industrial processes or safely released to the environment. 6. Conclusions Industrial ecology has focused on reusing waste and minimising energy loss between production systems, however, to date there has been no effective way to deal with large quantities of nutrient- or metal-rich wastewater. Freshwater macroalgae, exemplified by the genus Oedogonium, provide multiple opportunities for integration into agricultural, municipal and industrial systems to treat wastewater under a wide range of cultivation conditions and produce biomass with a diversity of end-uses. Ultimately any processes that can utilise waste streams to generate new products improve sustainability and reduce environmental impacts. The large-scale cultivation of freshwater macroalgae integrated into existing production systems will have significant benefits for both industry and the environment. Author contributions RL, NP and RdN conceived and designed the study; RL drafted the article; all authors critically revised the article and provided final approval of the version to be submitted; RdN provided funding. Acknowledgements This research is part of the MBD Energy Research and Development program for Biological Carbon Capture and Storage. This project was supported by the Australian Government through the Australian Renewable Energy Agency (ARENA) and the Advanced Manufacturing Cooperative Research Centre (AMCRC), funded through the Australian Government's Cooperative Research Centre Scheme. References [1] R.A. Frosch, Industrial ecology: a philosophical introduction, Proc. Natl. Acad. Sci. 89 (1992) 800–803. [2] E.A. Lowe, L.K. Evans, Industrial ecology and industrial ecosystems, J. Clean. Prod. 3 (1995) 47–53. [3] A. Nzihou, R. Lifset, Waste valorization, loop-closing, and industrial ecology, J. Ind. Ecol. 14 (2010) 196–199. [4] C. Scheel, Beyond sustainability. Transforming industrial zero-valued residues into increasing economic returns, J. Clean. Prod. 131 (2016) 376–386.
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[40]
[41]
[42] [43] [44]
[45]
[46] [47]
[48]
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Contents lists available at ScienceDirect
Algal Research journal homepage: www.elsevier.com/locate/algal
The industrial ecology of freshwater macroalgae for biomass applications Rebecca J. Lawton ⁎, Andrew J. Cole, David A. Roberts, Nicholas A. Paul, Rocky de Nys MACRO — the Centre for Macroalgal Resources and Biotechnology, James Cook University, Queensland 4811, Australia
a r t i c l e
i n f o
Article history: Received 1 December 2015 Received in revised form 24 August 2016 Accepted 30 August 2016 Available online xxxx Keywords: Oedogonium Bioremediation Biochar Bioenergy Wastewater Protein
a b s t r a c t Industrial ecology is focused on recognising the inherent value in waste streams and developing techniques that can efficiently recover this value. Freshwater macroalgae can become a foundation of this concept as they can be cultured in a range of waste streams where they can effectively remove excess nutrients, metals and metalloids, providing both a bioremediation service and a biomass resource. The cultured algal biomass can then be used as a product in animal feeds, biochar, biosorbents or as a feedstock biomass for the production of bioenergy. Freshwater macroalgae provide a unique opportunity to transform a range of industries through the utilisation of wastewater to produce biomass that can be converted into valuable bioproducts. © 2016 Published by Elsevier B.V.
1. Introduction
2. Large-scale cultivation of freshwater macroalgae in wastewater
Industrial ecology examines materials and energy flows in products, processes, industries and economies [1,2]. It aims to replicate the efficiencies seen in natural ecosystems and change industrial processes from linear systems, in which resources move through the system in a single direction to produce products and waste products, to systems where wastes are recycled to become inputs for new processes [1,3]. A central focus of industrial ecology is the development of processes and practices that reduce environmental impacts through the beneficial use of waste products as raw material [3] and is an innovative model for economic growth, social development and environmental management [4]. An innovative and developing industrial ecology model is to cultivate macroalgae in wastewater as a bioremediation technology, with the biomass then serving as an input for algal-based end-products such as food, feed, and bioenergy (e.g., [4]). Freshwater macroalgae provide a particularly innovative opportunity across multiple industries due to their ability to grow in a range of wastewaters and the suitability of resultant biomass for a variety of applications (Fig. 1). Our objective is to highlight and review recent research describing the large-scale cultivation of freshwater macroalgae in wastewater and their bioremediation capabilities, and provide an overview of the products which freshwater macroalgae can provide as a by-product of bioremediation. Finally, we demonstrate how freshwater macroalgae can be integrated into an industrial ecology system.
Large-scale cultivation of macroalgae in wastewater has predominantly occurred in algal turf scrubber (ATS) systems or open ponds at the scale of more than 20 kL day−1 (Table 1). ATS systems consist of an attached algal community, containing many species of macro- and microalgae and associated microbes and micro-invertebrates, which grows as a turf on screens in a shallow trough through which water is pumped [6]. The most widely used open pond system for large-scale macroalgal cultivation is the High Rate Algal Pond (HRAP) [4,7]. HRAPs are shallow, circular raceways around which water is gently circulated by a paddlewheel, maintaining the macroalgae in constant suspension. In contrast to ATS systems, which have a mixed algal community that is largely self-seeded and uncontrolled (e.g., [8]), HRAPs maintain a monoculture of a single species of macroalgae. This provides the advantage of delivering a consistent composition and source of biomass for bioproducts. Therefore, considerable research effort has focused on the identification of species of freshwater macroalgae for cultivation in outdoor pond systems. The macroalgal genera Rhizoclonium, Cladophora and Oedogonium have commonly been used for bioremediation [8–10]. However, it is clear that the cosmopolitan freshwater macroalgal genus Oedogonium has advantages in open pond systems as it is robust and competitively dominant with a biochemical composition which aligns itself well with a range of biomass applications ([11], Table 2). Oedogonium is an ideal candidate for use in an industrial ecology framework as it has high biomass productivities comparable to those of microalgae (~20 g dry weight (DW) m−2 day− 1) when cultured in a variety of water sources (Table 2), including agricultural and municipal wastewaters rich in nitrogen and phosphorus [9,12,13], and industrial wastewater
⁎ Corresponding author. E-mail address: [email protected] (R.J. Lawton).
http://dx.doi.org/10.1016/j.algal.2016.08.019 2211-9264/© 2016 Published by Elsevier B.V.
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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Fig. 1. Conceptual model of freshwater macroalgae integration in an industrial ecology system.
contaminated with heavy metals [14–17]. Additionally, it has broad environmental tolerances to temperature, nutrient concentration, salinity and water flow rate (Table 2), making it particularly suited to industrial scale cultivation where it can adapt to suit the local conditions without requiring industries to change operational protocols. There are many benefits to cultivating freshwater macroalgae in wastewater. A primary benefit is that macroalgae can be produced without using large volumes of quality freshwater, thereby reducing competition between algal production and conventional agricultural production [18,19]. Moreover, when cultivated in nutrient-rich wastewater, for example from agriculture production or municipal water treatment, freshwater macroalgae do not require any additional fertiliser inputs [10,12,20,21] reducing input costs. Cultivation of freshwater macroalgae in wastewater can provide an alternative treatment service, removing nutrients, metals and other contaminants from the wastewater (see Section 3). This also recovers nutrients or minerals in the wastewater that would otherwise be lost by using macroalgal biomass grown in wastewater as a biomass resource (see Section 4). However, there are also considerations in cultivating freshwater macroalgae in wastewater. Macroalgal biomass cultivated in wastewater contaminated with heavy metals or other toxins may be unsuitable for some biomass applications such as human and animal food, or agricultural fertiliser [23]. Similarly, if the composition of wastewater varies considerably over time, then the biochemical composition of freshwater macroalgae cultivated in this water can vary, making it unsuitable for
use in end product applications requiring algal biomass with a consistent biochemical composition. More generally the benefits and disadvantages of large scale algal cultivation of macroalgae require careful consideration, however, cultivation in wastewater alleviates some of the generic issues that have been raised in the broad scale production of microalgae, specifically contamination and harvesting [24]. 3. Bioremediation Freshwater macroalgae are highly successful at sequestering nutrients, metals and metalloids from wastewaters and in all cases the success of bioremediation is directly correlated to productivity, with increases in the growth of algae (productivity) resulting in increases in the bioremediation of contaminants [9,10,12,13,17,25,26]. As an example, for nutrient rich wastewater from agricultural production, a mixed algal species ATS system treating dairy manure had uptake rates of 0.40– 1.26 g m−2 day−1 for nitrogen and 0.06–0.22 g m−2 day−1 for phosphorus across a range of productivities from 2.5–24 g DW m−2 day−1 [10]. When cultured on-site in wastewater from an intensive freshwater fish farm, Oedogonium had comparable uptake rates of up to 0.45– 1.09 g m−2 day−1 for nitrogen and 0.08–0.13 g m−2 day−1 for phosphorus across a range of productivities from 3.8–23.8 g DW m−2 day−1 [12]. Similarly, when cultured in primary treated effluent from a municipal wastewater treatment facility, Oedogonium had stable uptake rates of up to 0.50 g m−2 day−1 for nitrogen and 0.11 g m−2 day−1 for
Table 1 Large scale cultivation of macroalgae in wastewater in Algal Turf Scrubber (ATS) systems and High Rate Algal Ponds (HRAP). System sizes are reported as length × width (m). Volume of water treated (volume) is reported as kL day−1; only systems treating N20 kL water per day have been included. FW: freshwater. Reference
Wastewater type
Type of algae used
System type
System size
Volume
[53] [10] [54] [52] [55] [51] [8] [56] [7]
Municipal, point source Dairy manure, point source Municipal, point source Municipal, point source Agriculture, non-point source Agriculture, non-point source Agriculture, non-point source Municipal, point source Aquaculture, point source
FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macro- and microalgae FW macroalgae Marine macroalgae
ATS ATS ATS ATS ATS ATS ATS HRAP HRAP
152 × 6.7 30 × 1 90 × 0.3 90 × 0.3 15.2 & 24.4 × 0.6 50 × 1 234 × 1.2 22 × 11 10 × 1
436–889 134 109 112–1080 55 137 327 36 36
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Table 2 Minimum and maximum reported values for environmental conditions that Oedogonium has been cultivated under, and biochemical characteristics of Oedogonium biomass. All studies which listed specific values for each parameter are noted in the References column. Minimum
Maximum
References
Cultivation conditions Temperature (°C) Water flow rate (volumes day−1) Light (mol photons m−2 day−1) Dissolved inorganic nitrogen (DIN) concentration (mg L−1) Reactive phosphorus concentration (mg L−1) Salinity (‰)
5.8 0 (batch culture) 4.3 0.66 0.2 0
32.1 5.0 60.4 23.1 4.1 3.0
[9,11,12,14–16,42,57,58] [9,11,12,14–17,35,36,39,41,42,57,58] [9,11–16,42,57,58] [9,11–13,16,41,57,58] [9,11–13,16,41,57,58] [58,59]
Biomass characteristics Biomass productivity (g DW m−2 day−1) Total protein (wt%) Essential amino acids (% total amino acid) Total lipids (wt%) Ash (wt%) Carbohydrates (wt%) Higher heating value (MJ kg−1)
1.9 4.0 43.1 7.9 2.9 41.0 15.8
40.0 34.0 43.7 9.4 43.7 41.0 20.1
[9,11–17,41,42,58] [9,12,39,40,58] [9,58] [39,58] [9,11,13,39,41,42,47,58,60] [39,58] [11,12,39–42,48,58]
phosphorus across a range of productivities from 6.8–9.9 g DW m−2 day−1 [13]. Notably, when cultured on-site in industrial wastewaters in open ponds, monocultures of Oedogonium had metal sequestration rates of 1 mg for every g of algal productivity (g DW m−2 day−1) and this uptake rate was consistent across a range of productivities, from 2.9– 10 g m−2 day−1 [17]. Oedogonium monocultures significantly improved water quality with the continuous production and harvest of biomass from ash water reducing the concentration of Al, As, Cd, Ni and Zn in this water from initial levels in excess of water quality criteria to levels meeting guidelines within 3–28 days [16,17]. 4. Products 4.1. Animal feed Freshwater macroalgae cultured in nutrient rich (N + P) wastewater from aquaculture or agricultural production provides a high quality source of protein and trace minerals, making this biomass an attractive alternative animal feed source/supplement. The protein content of freshwater macroalgae varies among species and with cultivation conditions, however, is comparable to terrestrial crops. For example, the crude protein content in biomass comprised of multiple species of freshwater macroalgae cultivated in dairy manure ranged from 31 to 44% DW (calcuated as N × 6.25, [21]), while the crude protein content in Oedogonium biomass cultivated in aquaculture wastewater ranged from 26 to 28% DW (calcuated using a species specific conversion factor of N × 4.7, [11]). The protein in Oedogonium is particularly attractive as just under half is composed of essential amino acids, with high concentrations of methionine and lysine. Moreover, the protein content of Oedogonium can be recovered rapidly following nutrient depletion if a pulse of nitrogen is applied [27]. Freshwater macroalgal biomass also contains a range of trace elements and minerals including Ca, K, P and Mg [8– 10], which are important for animal growth and development [28,29]. Compared to decorticated cottonseed meal (DCM), a valued protein supplement used in animal feed, freshwater macroalgae have a lower crude protein content and essential amino content, a comparable gross energy content, a higher total lipid content, a lower phosphorus content and a much higher sulfur content [30]. Notably, the properties of freshwater macroalgae biomass, in particular mineral, protein and lipid content, can be manipulated by varying cultivation conditions and post-harvest processing practices [9,31], providing a mechanism to tailor biomass to the specific nutritional requirements of different animals. 4.2. Soil ameliorants Freshwater macroalgae can be converted into soil ameliorants as slow-release fertilisers or carbon-rich biochar. Freshwater macroalgae
cultivated in wastewater from animal production is an effective slow release fertiliser when applied as untreated dried and milled biomass, with equivalent effects on plant mass and nutrient content to commercial fertiliser [32,33]. Biochar, the product of the combustion of algal biomass under oxygen-limiting conditions [34], produced from Oedogonium biomass improves the retention of nutrients from fertiliser (N, P, Ca, Mg, K and Mo) in low quality soils and enhances plant growth and nutrient uptake [23]. For example, radishes grown in low quality, sandy loam soils concurrently provided with fertiliser and biochar had 35–40% higher growth rates and much higher concentrations (10– 50%) of essential trace elements (Ca, Mg, K and Mo) and macro nutrients (P) compared to radishes grown with fertiliser but without biochar [23]. Importantly, the production of biochar through slow pyrolysis provides an opportunity to utilise biomass cultured in industrial wastewater as the pyrolysis process immobilises metals accumulated by live macroalgae in the resulting biochar with lower leachable concentrations of metals compared to the biomass [17,23]. 4.3. Biosorbents Biochar produced from freshwater macroalgae can also be used as a biosorbent that effectively binds metals [35,36]. Alternatively, the biomass can be treated with an iron (Fe) solution prior to conversion to biochar to produce a biosorbent that effectively binds metalloids [35– 37]. The sequential application of biochar and Fe-treated biochar can then be used to comprehensively remove metals and metalloids from a range of industrial wastewaters [36]. This provides a specific innovation in closing the loop for industrial wastewaters where macroalgae first provide a bioremediation service through the sequestration of metals and trace elements as they grow, and secondly through further re-use as biochar to continue the treatment process. Finally, this metal and trace element rich resource can be re-used, with consideration, in the remediation of stockpiled mine soils [38]. 4.4. Bioenergy Freshwater macroalgae cultured in any type of wastewater can be used as a bioenergy resource. Higher heating values (HHV, a measure of the amount of stored energy) for freshwater macroalgae biomass range from 12.1 MJ kg−1 for Pithophora to 22.3 MJ kg−1 for Spirogyra [11,39–42]. These values are comparable to those of the alternative bioenergy feedstocks of terrestrial crop residues (11–28 MJ kg− 1), wood (12 MJ kg−1) and the industrial biomass crop Miscanthus (18.5 MJ kg−1) [41,43]. Freshwater macroalgal biomass has been successfully converted to a range of biofuels with a focus on thermochemical processes to maximise the energy yield [44]. Oedogonium and Cladophora have high yields of biocrude (27% DW and 26.3% DW
Please cite this article as: R.J. Lawton, et al., The industrial ecology of freshwater macroalgae for biomass applications, Algal Res. (2016), http:// dx.doi.org/10.1016/j.algal.2016.08.019
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respectively) with high energy potential (HHV of 33.7 and 33.5 MJ kg−1 respectively) when processed using hydrothermal liquefaction [13,39]. Furthermore, the quality of the biocrude can be improved through selective post-harvest processing to reduce the quantities of heteroatoms (N + S) [31]. Cladophora and Oedogonium have been also been converted to biogas and bio-oil through slow and fast pyrolysis [40]. In alternative pathways to produce liquid fuels, Oedogonium has been used as a research scale feedstock for the production of biodiesel through the transesterification of extracted lipids [45]. However, freshwater macroalgae have a low lipid content making this process less applied at scale. In contrast, there is significant interest in the conversion of macroalgal biomass to ethanol, particularly given the biochemical composition of carbohydrates in green algae (chlorophyta), the predominant taxonomic grouping of freshwater macroalgae. For example, Spirogyra has been converted to bioethanol through fermentation [46]. Freshwater macroalgae biomass can be used as a combustible fuel [47]
and is also suitable for co-combustion with coal [48,49]. Freshwater macroalgae can also be converted to energy using biological processing through anaerobic digestion to methane and subsequent conversion to energy, most commonly through combustion. The anaerobic digestion of Rhizoclonium biomass produced 93–145 mL methane g DW−1, depending on pre-treatment methods [50]. This also provides the opportunity to deliver the closed loop re-capture of nitrogen and phosphorous as these are concentrated end-products in the wastewater from the anaerobic digestion process that are often an issue in terms of disposal. 5. Integration of freshwater macroalgae into industrial ecology systems Freshwater macroalgae provide a unique opportunity to transform a range of industries through the utilisation of wastewater streams to
A) Integrated agricultural production system
Agriculture
Waste water
Macroalgal cultivation
Feed mill
Animal production
Fertiliser
Crop production
Water re-use Clean water
Discharge
B) Integrated municipal waste production system
Municipal waste
Waste water
Macroalgal cultivation Biocrude
Refinery
Fertiliser
Crop production
Biofuel
Water re-use Clean water
Discharge
C) Integrated industrial production system
Industry Flue gas
Macroalgal cultivation Biochar
Waste water
Biocrude
Fertiliser
Refinery
Crop production
Biofuel
Water re-use Clean water
Discharge
Fig. 2. Conceptual model of integrated freshwater macroalgae production in A) agricultural systems, B) municipal waste systems and C) industrial systems.
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R.J. Lawton et al. / Algal Research xxx (2016) xxx–xxx
produce algal biomass that can be converted into valuable bioproducts. In agricultural systems, freshwater macroalgae can be cultivated on-site in nutrient rich wastewaters, resulting in an improvement to water quality and an accumulation of N, P and other minerals and trace elements in their biomass (Fig. 2A) [8,9,12,51]. This biomass can then be used as a high quality feed ingredient or slow release fertiliser, and the treated water from macroalgal cultures could be recycled back for re-use in animal production or industrial use. In municipal waste treatment systems, freshwater macroalgae can be cultivated on-site in nutrient rich wastewaters, reducing concentrations of dissolved nitrogen and phosphorus in the wastewater (Fig. 2B) [13]. The resultant biomass can then be converted into a range of bioenergy resources such as biocrude, biogas, bio-oil or ethanol [13,39–41] and the treated water from macroalgal cultures could be recycled back for re-use in municipal waste treatment or safely released to the environment. The biomass could also be converted to biochar and used as a soil ameliorant [23]. In industrial systems, freshwater macroalgae can be cultivated on-site in waste effluents, removing contaminants and treating water (Fig. 2C) [13,14,17,52]. The resultant biomass can then be dried or converted to biochar and used as a biosorbent to further treat these metal-rich wastewaters [35,36]. The biochar can also be used as an ameliorant for low-fertility soils, for example to aid in mine site rehabilitation [23]. Alternatively, the resultant biomass can be converted into a range of bioenergy resources such as biocrude [39–41]. Finally, treated water from macroalgal cultures can be recycled back for re-use in industrial processes or safely released to the environment. 6. Conclusions Industrial ecology has focused on reusing waste and minimising energy loss between production systems, however, to date there has been no effective way to deal with large quantities of nutrient- or metal-rich wastewater. Freshwater macroalgae, exemplified by the genus Oedogonium, provide multiple opportunities for integration into agricultural, municipal and industrial systems to treat wastewater under a wide range of cultivation conditions and produce biomass with a diversity of end-uses. Ultimately any processes that can utilise waste streams to generate new products improve sustainability and reduce environmental impacts. The large-scale cultivation of freshwater macroalgae integrated into existing production systems will have significant benefits for both industry and the environment. Author contributions RL, NP and RdN conceived and designed the study; RL drafted the article; all authors critically revised the article and provided final approval of the version to be submitted; RdN provided funding. Acknowledgements This research is part of the MBD Energy Research and Development program for Biological Carbon Capture and Storage. This project was supported by the Australian Government through the Australian Renewable Energy Agency (ARENA) and the Advanced Manufacturing Cooperative Research Centre (AMCRC), funded through the Australian Government's Cooperative Research Centre Scheme. References [1] R.A. Frosch, Industrial ecology: a philosophical introduction, Proc. Natl. Acad. Sci. 89 (1992) 800–803. [2] E.A. Lowe, L.K. Evans, Industrial ecology and industrial ecosystems, J. Clean. Prod. 3 (1995) 47–53. [3] A. Nzihou, R. Lifset, Waste valorization, loop-closing, and industrial ecology, J. Ind. Ecol. 14 (2010) 196–199. [4] C. Scheel, Beyond sustainability. Transforming industrial zero-valued residues into increasing economic returns, J. Clean. Prod. 131 (2016) 376–386.
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