Abstract
Energy has been playing a pivotal role in the progress and prosperity of a nation. Growing demands with dwindling stock of fossil fuels with the associated greenhouse gas (GHG) footprint and the consequent changes in the climate during the post-industrialization era have necessitated the exploration for sustainable energy alternatives. Biofuels are gaining importance as viable alternatives to fossil fuels during the last decade. Microalgae, especially diatoms, have shown prospects to be viable third-generation biofuel feedstocks, due to its higher lipid productivity, shorter cycling time and ubiquitous presence. This investigation focuses on identifying robust diatom strains that can sustain the vagaries of nature and yield higher lipid. This would avert the imminent risks of contamination associated with pure cultures and higher costs. The current research involved inventorying diatom consortia across diverse lentic and lotic habitats of the Aghanashini estuary with varied levels of nutrients primarily influenced by distribution of flora and fauna to understand the role of environmental parameters and nutrient levels in species composition, community structure. This effort is an essential prelude to phyco-prospecting potential candidates for third-generation biofuel production. The results obtained from the present study provide insights into an optimal habitat conditions, more specifically ideal nutrient concentrations for enhanced growth of different clusters of diatoms, a determining factor for higher biomass and lipid productivity. Multivariate statistical analyses revealed an occurrence of 27 tolerant diatoms species belonging to genera’s Amphora, Cyclotella, Navicula, Nitzschia and Pleurosigma. Linkages of the dominant and productive clusters of diatoms with habitat nutrient concentrations were investigated through agglomerative hierarchical clustering. Probable empirical relationship among varying environmental conditions and corresponding lipid content of diatoms were explored through regression analyses. Investigations of species tolerant to higher nutrient loads and assessment of lipid aided in prioritizing the strains with benefits of phyco-remediation as well as prospects of biofuel.
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References
Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saudi J Biol Sci 19:257–275
Abomohra AE-F, El-Sheekh M, Hanelt D (2017) Screening of marine microalgae isolated from the hypersaline Bardawil lagoon for biodiesel feedstock. Renew Energy 101:1266–1272
Alabaster JS, Lloyd R, Food and Agriculture Organization of the United Nations (1984) Water quality criteria for freshwater fish. Published by arrangement with the Food and Agriculture Organization of the United Nations by Butterworths
APHA (2005) American Public Health Association. Standard methods for the examination of water and wastewater. American Water Works Association. Water Environmental Federation
Badarudeen A, Damodaran KT, Sajan K, Padmalal D (1996) Texture and geochemistry of the sediments of a tropical mangrove ecosystem, southwest coast of India. Environ Geol 27:164–169
Balakrishnan S, Chelladurai G, Mohanraj J, Poongodi J (2017) Seasonal variations in physico-chemical characteristics of Tuticorin coastal waters, southeast coast of India. Appl Water Sci 7:1881–1886
Barclay W, Johansen J, Chelf P, Nagle N, Roessler P, Lemke P (2007) Microalgae culture collection 1986–1987. Solar Energy Research Institute, Golden
Besse-Lototskaya A, Verdonschot PFM, Coste M, Van de Vijver B (2011) Evaluation of European diatom trophic indices. Ecol Ind 11:456–467
Boominathan M, Chandran MDS, Ramachandra TV (2008) Economic valuation of bivalves in the Aghanashini Estuary, west coast, Karnataka. ENVIS technical report 48, centre for ecological sciences, indian institute of science, Bangalore, India, pp 22
Breuer F, Janz P, Farrelly E, Ebke P (2016) Seasonality of algal communities in small streams and ditches in temperate regions using delayed fluorescence. J Freshw Ecol 31:393–406
Chen Y-C (2012) The biomass and total lipid content and composition of twelve species of marine diatoms cultured under various environments. Food Chem 131:211–219
Chessman BC, Bate N, Gell PA, Newall P (2007) A diatom species index for bioassessment of Australian rivers. Mar Freshw Res 58:542
Chinnasamy S, Bhatnagar A, Claxton R, Das KC (2010) Biomass and bioenergy production potential of microalgae consortium in open and closed bioreactors using untreated carpet industry effluent as growth medium. Bioresour Technol 101:6751–6760
Chu W-L (2017) Strategies to enhance production of microalgal biomass and lipids for biofuel feedstock. Eur J Phycol 52:419–437
Cumming G (2013) Understanding the new statistics. Routledge, New York
D’Costa PM, Anil AC (2010) Diatom community dynamics in a tropical, monsoon-influenced environment: West coast of India. Cont Shelf Res 30:1324–1337
D’Ippolito G, Tucci S, Cutignano A, Romano G, Cimino G, Miralto A, Fontana A (2004) The role of complex lipids in the synthesis of bioactive aldehydes of the marine diatom Skeletonema costatum. Biochim Biophys Acta Mol Cell Biol Lipids 1686:100–107
D’Ippolito G, Sardo A, Paris D, Vella FM, Adelfi MG, Botte P, Gallo C, Fontana A (2015) Potential of lipid metabolism in marine diatoms for biofuel production. Biotechnol Biofuels 8:28
Dares (2004) 4. Enumeration of diatom samples. Diatoms for assessing river ecological status (DARES), pp 1–13. http://craticula.ncl.ac.uk/dares/methods.htm. Accessed Feb 2018
De Clerck O, Guiry MD, Leliaert F, Samyn Y, Verbruggen H (2013) Algal taxonomy: a road to nowhere? J Phycol 49:215–225
De La Peña MR (2007) Cell growth and nutritive value of the tropical benthic diatom, Amphora sp., at varying levels of nutrients and light intensity, and different culture locations. J Appl Phycol 19:647–655
Delgado C, Pardo I, García L (2012) Diatom communities as indicators of ecological status in Mediterranean temporary streams (Balearic Islands, Spain). Ecol Ind 15:131–139
Demirtas H (2018) Handbook of fitting statistical distributions with R. CRC Press, Boca Raton
Desrosieres R (1969) Surface macroplankton of the Pacific Ocean along the Equator. Limnol Oceanogr 14:626–632
Fatema K, Wan Maznah WO, Isa MM (2014) Spatial and temporal variation of physico-chemical parameters in the Merbok Estuary, Kedah, Malaysia. Trop Life Sci Res 25:1–19
Fields FJ, Kociolek JP (2015) An evolutionary perspective on selecting high-lipid-content diatoms (Bacillariophyta). J Appl Phycol 27:2209–2220
Fore LS, Grafe C (2002) Using diatoms to assess the biological condition of large rivers in Idaho (U.S.A.). Freshw Biol 47:2015–2037
Fu W, Wichuk K, Brynjólfsson S (2015) Develo** diatoms for value-added products: challenges and opportunities. New Biotechnol 32:547–551
George B, Nirmal Kumar JI, Kumar RN (2012) Study on the influence of hydro-chemical parameters on phytoplankton distribution along Tapi estuarine area of Gulf of Khambhat, India. Egypt J Aquat Res 38:157–170
Godhantaraman N (2002) Seasonal variations in species composition, abundance, biomass and estimated production rates of tintinnids at tropical estuarine and mangrove waters, Parangipettai, southeast coast of India. J Mar Syst 36:161–171
Graham JM, Graham LE, Zulkifly SB, Pfleger BF, Hoover SW, Yoshitani J (2012) Freshwater diatoms as a source of lipids for biofuels. J Ind Microbiol Biotechnol 39:419–428
Grobbelaar JU (2009) Factors governing algal growth in photobioreactors: the “open” versus “closed” debate. J Appl Phycol 21:489–492
Hammer DAT, Ryan PD, Hammer Ø, Harper DAT (2001) Past: paleontological statistics software package for education and data analysis. https://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed Feb 2018
Hausmann S, Charles DF, Gerritsen J, Belton TJ (2016) A diatom-based biological condition gradient (BCG) approach for assessing impairment and develo** nutrient criteria for streams. Sci Total Environ 562:914–927
Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R (2012) The place of diatoms in the biofuels industry. Biofuels 3:221–240
Huesemann MH, Van Wagenen J, Miller T, Chavis A, Hobbs S, Crowe B (2013) A screening model to predict microalgae biomass growth in photobioreactors and raceway ponds. Biotechnol Bioeng 110:1583–1594
Idris NA, Loh SK, Lau HLN, Yau TC, Mustafa EM, Vello V, Moi PS (2018) Palm oil mill effluent as algae cultivation medium for biodiesel production. J Oil Palm Res 30:141–149
Juahir H, Zain SM, Yusoff MK, Hanidza TIT, Armi ASM, Toriman ME, Mokhtar M (2011) Spatial water quality assessment of Langat River Basin (Malaysia) using environmetric techniques. Environ Monit Assess 173:625–641
Kamyab H, Din MFM, Ghoshal SK, Lee CT, Keyvanfar A, Bavafa AA, Rezania S, Lim JS (2016) Chlorella pyrenoidosa mediated lipid production using Malaysian agricultural wastewater: effects of photon and carbon. Waste Biomass Valoriz 7:779–788
Karthick B, Hamilton PB, Kociolek JP (2013) An illustrated guide to common diatoms of peninsular India. Ashoka trust for research in ecology and the environment. Bangalore, pp 145
Kelly MG, Whitton BA (1995) Trophic diatoms index—a new index for monitoring eutrophication in rivers. J Appl Phycol 7:433–444
Krammer K, Bertolet H (1986) Bacillariophyceae. 1. Teil: Naviculaceae In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa, Band 2/1. Stuttgart — New York, Fischer Verlag, pp 178
Krzywinski M, Altman N (2013) Significance, P values and t-tests. Nat Methods 10:1041–1042
Kumar TS (2008) Sewage/effluent treatment by growth of diatom algae current practices. Probl Curr Pract 1–7. http://www.indiawaterportal.org/sites/indiawaterportal.org/files/uploads/2008/07/nualgi_final1udaipur-conference.pdf. Accessed 12 March 2018
Levinton JS (2017) Marine biology: function, biodiversity, ecology, 5th edn. Oxford University Press, Pp 592
Levitan O, Dinamarca J, Hochman G, Falkowski PG (2014) Diatoms: a fossil fuel of the future. Trends Biotechnol 32:117–124
Linkins AE (1973) Uptake and utilization of glucose and acetate by a marine chemoorganotrophic diatom Nitzschia alba Clone Link 001. University of Massachusetts, Amherst
Liu A, Chen W, Zheng L, Song L (2011) Identification of high-lipid producers for biodiesel production from forty-three green algal isolates in China. Progr Nat Sci Mater Int 21:269–276
Madhu NV, Jyothibabu R, Balachandran KK, Honey UK, Martin GD, Vijay JG, Shiyas CA, Gupta GVM, Achuthankutty CT (2007) Monsoonal impact on planktonic standing stock and abundance in a tropical estuary (Cochin backwaters—India). Estuar Coast Shelf Sci 73:54–64
Mahapatra DM, Chanakya HN, Ramachandra TV (2014) Bioremediation and lipid synthesis through mixotrophic algal consortia in municipal wastewater. Bioresour Technol 168:142–150
Mann KH (2000) Ecology of coastal waters: with implications for management, 2nd edn. Wiley, Hoboken. ISBN 978-0-865-42550-7
Marella TK, Parine NR, Tiwari A (2017) Potential of diatom consortium developed by nutrient enrichment for biodiesel production and simultaneous nutrient removal from waste water. Saudi J Biol Sci 25:704–709
Martin GD, Vijay JG, Laluraj CM, Madhu NV, Joseph T, Nair M, Gupta GVM, Balachandran KK (2008) Fresh water influence on nutrient stoichiometry in a tropical estuary, Southwest coast of India. Appl Ecol Environ Res 6(1):57–64
Martin GD, Nisha PA, Balachandran KK, Madhu NV, Nair M, Shaiju P, Joseph T, Srinivas K, Gupta GVM (2011) Eutrophication induced changes in benthic community structure of a flow-restricted tropical estuary (Cochin backwaters), India. Environ Monit Assess 176:427–438
Millero FJ (1986) The pH of estuarine waters. Limnol Oceanogr 31:839–847
Mitbavkar S, Anil AC (2008) Seasonal variations in the fouling diatom community structure from a monsoon influenced tropical estuary. Biofouling 24:415–426
Nabout JC, Nogueira IS, Oliveira LG (2006) Phytoplankton community of flood plain lakes of the Araguaia River, Brazil, in the rainy and dry seasons. J Plankton Res 28:181–193
Ouyang Y, Nkedi-Kizza P, Wu QT, Shinde D, Huang CH (2006) Assessment of seasonal variations in surface water quality. Water Res 40:3800–3810
Pan Y, Stevenson RJ, Hill BH, Herlihy AT, Collins GB (1996) Using diatoms as indicators of ecological conditions in lotic systems: a regional assessment. J N Am Benthol Soc 15:481–495
Patrick R, Reimer CW (1966) The diatoms of the United States. Monogr Acad Nat Sci Phila 1(13):1–688
Potapova MG, Charles DF (2002) Benthic diatoms in USA rivers: distributions along spatial and environmental gradients. J Biogeogr 29:167–187
Potapova M, Charles DF (2007) Diatom metrics for monitoring eutrophication in rivers of the United States. Ecol Ind 7:48–70
Prabu VA, Rajkumar M, Perumal P (2008) Seasonal variations in physico-chemical characteristics of Pichavaram mangroves, southeast coast of India. J Environ Biol 29:945–950
Ramachandra TV, Mahapatra DM, Karthick B, Gordon R (2009) Milking diatoms for sustainable energy: biochemical engineering versus gasoline-secreting diatom solar panels. Ind Eng Chem Res 48:8769–8788
Ramachandra TV, Durga Madhab M, Shilpi S, Joshi NV (2013) Algal biofuel from urban wastewater in India: scope and challenges. Renew Sustain Energy Rev 21:767–777
Ramachandra TV, Mahapatra DM, Bhat SP, Joshi NV (2015) biofuel production along with remediation of sewage water through algae. In: Singh B, Bauddh K, Bux F (eds) Algae and environmental sustainability. Springer, New Delhi, pp 33–51
Rath AR, Mitbavkar S, Anil AC (2018) Phytoplankton community structure in relation to environmental factors from the New Mangalore Port waters along the southwest coast of India. Environ Monit Assess 190:481
Richardson TL, Gibson CE, Heaney SI (2000) Temperature, growth and seasonal succession of phytoplankton in Lake Baikal, Siberia. Freshw Biol 44:431–440
Rimet F (2009) Benthic diatom assemblages and their correspondence with ecoregional classifications: case study of rivers in north-eastern France. Hydrobiologia 636:137–151
Round FE (1991) Diatoms in river water-monitoring studies. J Appl Phycol 3:129–145
Satpathy KK, Mohanty AK, Natesan U, Prasad MVR, Sarkar SK (2010) Seasonal variation in physicochemical properties of coastal waters of Kalpakkam, east coast of India with special emphasis on nutrients. Environ Monit Assess 164:153–171
Schoeman FR (1972) A further contribution to the diatom flora of sewage enriched waters in southern Africa. Phycologia 11:239–245
Schoeman FR (1979) Diatoms as indicators of water quality in the Upper Hennops River (Transvaal, South Africa). J Limnol Soc S Afr 5:73–78
Scholz B, Liebezeit G (2013) Biochemical characterisation and fatty acid profiles of 25 benthic marine diatoms isolated from the Solthörn tidal flat (southern North Sea). J Appl Phycol 25:453–465
Sforza E, Bertucco A, Morosinotto T, Giacometti GM (2012) Photobioreactors for microalgal growth and oil production with Nannochloropsis salina: from lab-scale experiments to large-scale design. Chem Eng Res Des 90:1151–1158
Shah MR, Hossain MY, Begum M, Ahmed ZF, Ohtomi J, Rahman MM, Alam MJ, Islam MA, Fulanda B (2008) Seasonal variations of phytoplanktonic community structure and production in relation to environmental factors of the southwest coastal waters of Bangladesh. J Fish Aquat Sci 3:102–113
Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. Department of Energy’s Aquatic Species Program: biodiesel from algae, National Renewable Energy Laboratory, US Department of Energy, 1998. http://www1.eere.energy.gov/biomass/pdfs/biodiesel_from_algae.pdf. Accessed 12 March 2018
Simonsen R (1968) RUTH PATRICK und CH. W. REIMER: the diatoms of the United States. Vol. I. Mono graphs of the Academy of Natural Sciences of Philadelphia, 13, xi + 688 pp., 64 Taf., Philadelphia, 1966, U.S. $6 18,50. Internationale Revue der gesamten Hydrobiologie und Hydrographie 53:166–167
Soininen J, Eloranta R, Muotka T (2004) Benthic diatom community structure in boreal streams. Ecography 27:330–344
Stevenson RJ (1997) Scale-dependent determinants and consequences of benthic algal heterogeneity. J N Am Benthol Soc 16:248–262
Stevenson RJ, Bothwell ML, Lowe RL (1996) Algal ecology: freshwater benthic ecosystems. Academic Press, New York
Sumich JL, Morrissey JF (2004) Introduction to the biology of marine life. Jones and Bartlett Publishers, Burlington
Tan X, **a X, Zhao Q, Zhang Q (2014) Temporal variations of benthic diatom community and its main influencing factors in a subtropical river, China. Environ Sci Pollut Res 21:434–444
Tan X, Zhang Q, Burford MA, Sheldon F, Bunn SE (2017) Benthic diatom based indices for water quality assessment in two subtropical streams. Front Microbiol 8:601
Tang D, Han W, Li P, Miao X, Zhong J (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresour Technol 102:3071–3076
Tang H, Chen M, Simon Ng KY, Salley SO (2012) Continuous microalgae cultivation in a photobioreactor. Biotechnol Bioeng 109:2468–2474
Taylor JC, Harding WR, Archibald CGM (2007) A methods manual for the collection, preparation and analysis of diatom samples (WRC Report TT 281/07), Koeltz Botanical Books, Germany, pp 410
Taylor JC, Prygiel J, Vosloo A, de la Rey PA, van Rensburg L (2007b) Can diatom-based pollution indices be used for biomonitoring in South Africa? A case study of the Crocodile West and Marico water management area. Hydrobiologia 592:455–464
Townsend SA, Gell PA (2005) The role of substrate type on benthic diatom assemblages in the Daly and Roper Rivers of the Australian Wet/Dry Tropics. Hydrobiologia 548:101–115
Underwood GJC, Paterson DM (1993) Seasonal changes in diatom biomass, sediment stability and biogenic stabilization in the Severn Estuary. J Mar Biol Assoc UK 73:871
van Aken HM (2008) Variability of the water temperature in the western Wadden Sea on tidal to centennial time scales. J Sea Res 60:227–234
Van Heurck H (1896) A treatise on the diatomaceae. Translated by W.E. Baxter. Citations—diatoms of North America
Venkatesan R, Vasagam KPK, Balasubramanian T (2006) Culture of marine microalgae in shrimp farm discharge water: a sustainable approach to reduce the cost production and recovery of nutrients. J Fish Aquat Sci 1:262–269
Vinayak V, Manoylov K, Gateau H, Blanckaert V, Hérault J, Pencréac’h G, Marchand J, Gordon R, Schoefs B (2015) Diatom milking: a review and new approaches. Mar Drugs 13:2629–2665
Weilhoefer CL, Pan Y (2006) Diatom assemblages and their associations with environmental variables in Oregon Coast Range streams, USA. Hydrobiologia 561:207–219
Werner D (1977) The biology of diatoms. University of California Press, Berkeley
Widjaja A, Chien C-C, Ju Y-H (2009) Study of increasing lipid production from fresh water microalgae Chlorella vulgaris. J Taiwan Inst Chem Eng 40:13–20
Wiley P, Harris L, Reinsch S, Tozzi S, Embaye T, Clark K, McKuin B, Kolber Z, Adams R, Kagawa H, Richardson T-MJ, Malinowski J, Beal C, Claxton MA, Geiger E, Rask J, Campbell JE, Trent JD (2013) Microalgae cultivation using offshore membrane enclosures for growing algae (OMEGA). J Sustain Bioenergy Syst 03:18–32
Yin K (2002) Monsoonal influence on seasonal variations in nutrients and phytoplankton biomass in coastal waters of Hong Kong in the vicinity of the Pearl River estuary. Mar Ecol Progr Ser 245:111–122
Yusuf C (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306
Zhao F, Liang J, Gao Y, Luo Q, Yu Y, Chen C, Sun L (2016) Variations in the total lipid content and biological characteristics of diatom species for potential biodiesel production. Fundam Renew Energy Appl 6:22–26
Acknowledgements
We are grateful to (1) Gajanana and Madhavi Hegde endowment for biofuel research for the financial support and (2) the NRDMS Division, The Ministry of Science and Technology, Government of India; (3) Indian Institute of Science for the infrastructure support.
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Appendix
Appendix
- AB:
-
Achnanthes brevipes
- AOB:
-
Achnanthes oblongella
- ACS:
-
Achnanthes sp.
- AA:
-
Amphiprora alata
- AMPL:
-
Amphipleura pellucida
- AA:
-
Amphiprora alata
- AP1:
-
Amphiprora paludosa
- ACF:
-
Amphora coffeaeformis
- ACYM:
-
Amphora cymbifera
- AO1:
-
Amphora ovalis
- APR:
-
Amphora proteus
- ASL:
-
Amphora salina
- AMP:
-
Amphora sp.
- BP:
-
Bacillaria paradoxa
- BC:
-
Bacteriastum cosmosum
- CHT:
-
Chaetoceros sp.
- CPL:
-
Cocconeis pelta
- CEX:
-
Coscinodiscus excentricus
- CR:
-
Coscinodiscus radiatus
- CS:
-
Coscinodiscus subtilis
- CM:
-
Cyclotella meneghiniana
- CO:
-
Cyclotella operculata
- CYSO:
-
Cymatopleura solea
- CCYM:
-
Cymbella cymbiformis
- CYM:
-
Cymbella sp
- DO:
-
Diploneis ovalis
- DS:
-
Diploneis smithi
- EAR:
-
Epithema argus
- EG:
-
Epithema gibberula
- EPC:
-
Eunotia pectinalis
- EUN:
-
Eunotia sp.
- FAS:
-
Frustulia asiatica
- GG:
-
Gomphonema gracile
- GE:
-
Gyrosigma eximum
- GM:
-
Gyrosigma macrum
- GO:
-
Gyrosigma obscurum
- LT:
-
Licomophora tincta
- ML:
-
Mastogloia lanceolata
- MJ:
-
Melosira jurgensii
- MLI:
-
Melosira lineatus
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Saranya, G., Subashchandran, M.D., Mesta, P. et al. Prioritization of prospective third-generation biofuel diatom strains. Energ. Ecol. Environ. 3, 338–354 (2018). https://doi.org/10.1007/s40974-018-0105-z
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DOI: https://doi.org/10.1007/s40974-018-0105-z