Abstract
Algal bioremediation can significantly improve the quality of wastewater by assimilating nutrients. However, the efficiency and stability of this approach depends on identifying suitable algae based on their biomass productivity and ability to outcompete less desirable algae. Here, we compare the productivity and competitive ability of three taxa of filamentous macroalgae under the seasonal light and temperature conditions experienced in temperate environments, including extremes of heat and cold. Specific growth rate was greatest for the tropical isolate of Oedogonium under summer conditions (36–40%; P < 0.05); however, it had lower growth under cooler (autumn, winter) conditions than the temperate algae of Stigeoclonium and Hyalotheca. Overall, Stigeoclonium and Hyalotheca had the most stable production across all treatments. A 5-week competition experiment found that each algae grew fastest in monoculture compared with bi-culture and poly-culture treatments. While all three genera showed a considerable level of competitive dominance depending on algae composition and environmental conditions, no single genus outperformed all others under all conditions. Oedogonium was dominant in warmer conditions, Stigeoclonium in cooler conditions (> 90% for both) and, in its absence, Hyalotheca also dominate over Oedogonium. Our results suggest that rather than finding an optimal taxon for all four seasons, the best decision for maximising stable biomass production will require either seasonal rotation of algae, or bi-cultures of the most dominant ones. Further, prioritising competition over production when selecting freshwater algae for wastewater bioremediation is likely to prove the most successful strategy.
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References
Balina K, Romagnoli F, Pastare L, Blumberga D (2017) Use of macroalgae for bioenergy production in Latvia: review on potential availability of marine coastline species. Energy Procedia 113:403–410
Bruhn A, Dahl J, Nielsen HB, Nikolaisen L, Rasmussen MB, Markager S, Olesen B, Arias C, Jensen PD (2011) Bioenergy potential of Ulva lactuca: biomass yield, methane production and combustion. Bioresour Technol 102:2595–2604
Butterwick C, Heaney S, Talling J (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50:291–300
Channiwala S, Parikh P (2002) A unified correlation for estimating HHV of solid, liquid and gaseous fuels. Fuel 81:1051–1063
Clarens AF, Resurreccion EP, White MA, Colosi LM (2010) Environmental life cycle comparison of algae to other bioenergy feedstocks. Environ Sci Technol 44:1813–1819
Cole AJ, de Nys R, Paul NA (2014a) Removing constraints on the biomass production of freshwater macroalgae by manipulating water exchange to manage nutrient flux. PLoS One 9:e101284
Cole AJ, Mata L, Paul NA, de Nys R (2014b) Using CO2 to enhance carbon capture and biomass applications of freshwater macroalgae. GCB Bioenergy 6:637–645
Cole A, Dinburg Y, Haynes BS, He Y, Herskowitz M, Jazrawi C, Landau M, Liang X, Magnusson M, Maschmeyer T, Masters AF, Meiri N, Neveux N, de Nys R, Paul NA, Rabaev M, Vidruk-Nehemyab R, Yuen AKL (2016a) From macroalgae to liquid fuel via waste-water remediation, hydrothermal upgrading, carbon dioxide hydrogenation and hydrotreating. Energy Environ Sci 9:1828–1840
Cole AJ, Neveux N, Whelan A, Morton J, Vis M, de Nys R, Paul NA (2016b) Adding value to the treatment of municipal wastewater through the intensive production of freshwater macroalgae. Algal Res 20:100–109
Cole AJ, Paul NA, De Nys R, Roberts DA (2017) Good for sewage treatment and good for agriculture: algal based compost and biochar. J Environ Manag 200:105–113
Cole A, Praeger C, Mannering T, de Nys R, Magnusson M (2018) Hot and bright: thermal and light environments for the culture of Oedogonium intermedium and the geographical limits for large-scale cultivation in Australia. Algal Res 34:209–216
Colglazier W (2015) Sustainable development agenda: 2030. Science 349:1048–1050
Creel L (2003) Ripple effects: population and coastal regions. Population Reference Bureau Washington, DC: Population Reference Bureau and Measure Communication:1–7
Day SA, Wickham R, Entwisle TJ, Tyler P (1995) Bibliographic checklist of non-marine algae in Australia. vol 4. CSIRO, Canberra
Demirbas A (2010) Use of algae as biofuel sources. Energy Convers Manag 51:2738–2749
Entwisle TJ, Sonneman JA, Lewis SH (1997) Freshwater algae in Australia. Sainty & Associates, Sydney
Fortes M, Lüning K (1980) Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgoländer Meeresun 34:15–29
Garcia-Vaquero M, Hayes M (2016) Red and green macroalgae for fish and animal feed and human functional food development. Food Rev Int 32:15–45
Ge SJ, Madill M, Champagne P (2018) Use of freshwater macroalgae Spirogyra sp for the treatment of municipal wastewaters and biomass production for biofuel applications. Biomass Bioenergy 111:213–223
Goldman JC, Ryther JH (1975) Mass production of marine algae in outdoor cultures. Nature 254:594–595
Gonen Y, Kimmel E, Friedlander M (1993) Effect of relative water motion on photosynthetic rate of red alga Gracilaria conferta. Hydrobiologia 260:493–498
Grigg NS (2012) Water, wastewater, and stormwater infrastructure management. CRC Press, Boca Raton
Holdren JP, Ehrlich PR (1974) Human population and the global environment: population growth, rising per capita material consumption, and disruptive technologies have made civilization a global ecological force. Am Sci 62:282–292
Hossain AS, Salleh A, Boyce AN, Chowdhury P, Naqiuddin M (2008) Biodiesel fuel production from algae as renewable energy. Am J Biochem Biotechnol 4:250–254
Hughes AD, Kelly MS, Black KD, Stanley MS (2012) Biogas from Macroalgae: is it time to revisit the idea? Biotechnol Biofuels 5:86
Hurd C (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472
Kimor B (1992) The impact of eutrophication on phytoplankton composition in coastal marine ecosystems. In: Vollenweider RA, Marchetti R, Viviani R (eds) Marine coastal eutrophication. Elsevier, Amsterdam, pp 871–878
Lawton RJ, de Nys R, Paul NA (2013) Selecting reliable and robust freshwater macroalgae for biomass applications. PLoS One 8:e64168
Lawton RJ, de Nys R, Skinner S, Paul NA (2014) Isolation and identification of Oedogonium species and strains for biomass applications. PLoS One 9:e90223
Lawton RJ, Cole AJ, Roberts DA, Paul NA, de Nys R (2017) The industrial ecology of freshwater macroalgae for biomass applications. Algal Res 24:486–491
Lu QM, Knudsen JF, Eskesen SK, Powers JT, Shremp F, Segar DA, Stamman E, Yucheng Z (2012) Wastewater management for coastal cities: the ocean disposal option. Springer, Berlin
Martine G, Marshall A (2007) State of world population 2007: unleashing the potential of urban growth. UNFPA
Neveux N, Yuen AKL, Jazrawi C, Magnusson M, Haynes BS, Masters AF, Montoya A, Paul NA, Maschmeyer T, De Nys R (2014) Biocrude yield and productivity from the hydrothermal liquefaction of marine and freshwater green macroalgae. Bioresour Technol 155:334–341
Neveux N, Magnusson M, Maschmeyer T, de Nys R, Paul NA (2015) Comparing the potential production and value of high-energy liquid fuels and protein from marine and freshwater macroalgae. GCB Bioenergy 7:673–689
Neveux N, Magnusson M, Mata L, Whelan A, de Nys R, Paul NA (2016) The treatment of municipal wastewater by the macroalga Oedogonium sp. and its potential for the production of biocrude. Algal Res 13:284–292
Nzihou A, Lifset R (2010) Waste valorization, loop-closing, and industrial ecology. J Ind Ecol 14:196–199
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790
Pelling M, Blackburn S (2014) Megacities and the coast. Earthscan from Routledge, Oxford
Priyadarshani I, Sahu D, Rath B (2012) Algae in aquaculture. IJHS 2:108–114
Rabalais NN, Turner RE, Diaz RJ, Justić D (2009) Global change and eutrophication of coastal waters. ICES J Mar Sci 66:1528–1537
Roberts DA, de Nys R, Paul NA (2013) The effect of CO2 on algal growth in industrial waste water for bioenergy and bioremediation applications. PLoS One 8:e81631
y Royo CL, Silvestri C, Pergent G, Casazza G (2009) Assessing human-induced pressures on coastal areas with publicly available data. J Environ Manag 90:1494–1501
Shukla SK, Pandey P, Yoo K (2019) Commercial potential of phycoremediation of wastewater: a way forward. In: Gupta SK, Bux F (eds) Application of microalgae in wastewater treatment, Biorefinery approaches of wastewater treatment, vol 2. Springer, Cham, pp 215–231
Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut Res 10:126–139
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499
Wett B, Buchauer K, Fimml C (2007) Energy self-sufficiency as a feasible concept for wastewater treatment systems. In: IWA Leading Edge Technology Conference. Singapore: Asian Water, pp 21–24
Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser :283-292
Wilkie AC, Mulbry WW (2002) Recovery of dairy manure nutrients by benthic freshwater algae. Bioresour Technol 84:81–91
Wright LD, Syvitski J, Nichols CR (2019) Coastal systems in the anthropocene. In: Wright LD, Nichols CR (eds) Tomorrow’s coasts: complex and impermanent. Springer, Cham, pp 85–99
Yun J-H, Smith VH, deNoyelles FJ, Roberts GW, Stagg-Williams SM (2014) Freshwater macroalgae as a biofuels feedstock: mini-review and assessment of their bioenergy potential. Ind Biotechnol 10:212–220
Zhu Y, Kwong CW, van Eyk PJ, de Nys R, Wang D, Ashman PJ (2015) Pyrolysis characteristics and char reactivity of Oedogonium sp. and Loy Yang coal. Energy Fuel 29:5047–5055
Acknowledgements
We thank Maria Martínez, Rebecca Lawton and Tine Carl for their assistance with experiments and Melbourne Water and Melbourne City Council for allowing collection of algae from their ponds. This research is part of the Pacific Biotechnology (previously MBD Industries Ltd) Research and Development program for the Integrated Production of Macroalgae.
Funding
Funding was provided by the Australian Research Council through a Future Fellowship (TD) and by the Victorian Goverment through the Port Phillip Bay fund (SS).
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Valero-Rodriguez, J.M., Swearer, S.E., Dempster, T. et al. Evaluating the performance of freshwater macroalgae in the bioremediation of nutrient-enriched water in temperate environments. J Appl Phycol 32, 641–652 (2020). https://doi.org/10.1007/s10811-019-01908-4
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DOI: https://doi.org/10.1007/s10811-019-01908-4