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Marine Biotechnology

, Volume 19, Issue 4, pp 328–344 | Cite as

Molecular Identification and Comparative Evaluation of Tropical Marine Microalgae for Biodiesel Production

  • Sanyo Sabu
  • I.S. Bright Singh
  • Valsamma JosephEmail author
Original Article

Abstract

Marine microalgae have emerged as important feedstock for liquid biofuel production. The identification of lipid-rich native microalgal species with high growth rate and optimal fatty acid profile and biodiesel properties is the most challenging step in microalgae-based biodiesel production. In this study, attempts have been made to bio-prospect the biodiesel production potential of marine and brackish water microalgal isolates from the west coast of India. A total of 14 microalgal species were isolated, identified using specific molecular markers and based on the lipid content; seven species with total lipid content above 20% of dry cell weight were selected for assessing biodiesel production potential in terms of lipid and biomass productivities, nile red fluorescence, fatty acid profile and biodiesel properties. On comparative analysis, the diatoms were proven to be promising based on the overall desirable properties for biodiesel production. The most potential strain Navicula phyllepta MACC8 with a total lipid content of 26.54 % of dry weight of biomass, the highest growth rate (0.58 day−1) and lipid and biomass productivities of 114 and 431 mgL−1 day−1, respectively, was rich in fatty acids mainly of C16:0, C16:1 and C18:0 in the neutral lipid fraction, the most favoured fatty acids for ideal biodiesel properties. The biodiesel properties met the requirements of fuel quality standards based on empirical estimation. The marine diatoms hold a great promise as feedstock for large-scale biodiesel production along with valuable by-products in a biorefinery perspective, after augmenting lipid and biomass production through biochemical and genetic engineering approaches.

Keywords

Marine microalgae Molecular marker Lipid Fatty acid Biodiesel 

Notes

Acknowledgements

The authors acknowledge University Grants Commission, Government of India for the financial support under the major research grant [File No. F.No.41 568/2012(SR)], Centre for Marine Living Resources and Ecology, Ministry of Earth Sciences, India for facilitating cruises on board FORV Sagar Sampada, Postgraduate students from National Centre for Aquatic Animal Health for collecting marine microalgal samples from the west coast of India and Physics research lab, Maharaja’s college, Kochi, India for providing the scanning electron microscopy facility.

Supplementary material

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References

  1. A.O.A.C (1996) Official methods of analysis of AOAC international, 16th edn. Association of official analytical chemists, Washington DCGoogle Scholar
  2. Abdel-Hamid MI, El-Refaay DA, Abdel-Mogib M, Azad YA (2013) Studies on biomass and lipid production of seven diatom species with special emphasis on lipid composition of Nitzschia palea (bacillariophyceae) as reliable biodiesel feedstock. Algol Stud 143:65–87Google Scholar
  3. Acien FG, Camacho FG, Perez JAS, Sevilla JMF, Grima EM (1998) Modelling of biomass productivity in tubular photobioreactors for microalgal cultures: Effects of dilution rate, tube diameter and solar irradiance. Biotechnol Bioeng 58:605–616CrossRefGoogle Scholar
  4. Akgul R, Kizilkaya B, Akgul F, Erdugan H (2015) Total lipid and fatty acid composition of twelve algae from Canakkale (Turkey). Indian J Geomarine Sci 44:495–500Google Scholar
  5. Alonso L, Grima EM, Pérez JS, Sánchez JG, Camacho FG (1992) Fatty acid variation among different isolates of a single strain of Isochrysis galbana. Phytochemistry 31:3901–3904CrossRefGoogle Scholar
  6. Amaro HM, Macedo AC, Malcata FX (2012) Microalgae: An alternative as sustainable source of biofuels? Energy 44:158–166CrossRefGoogle Scholar
  7. Apt KE, Behrens PW (1999) Commercial developments in microalgal biotechnology. J Phycol 35:215–226CrossRefGoogle Scholar
  8. Beal CM, Gerber LN, Sills DL, Huntley ME, Machesky SC, Walsh MJ, Tester JW, Archibald I, Granados J, Greene CH (2015) Algal biofuel production for fuels and feed in a 100-ha facility: A comprehensive techno-economic analysis and life-cycle assessment. Algal Res 10:266–279CrossRefGoogle Scholar
  9. Becker EW (1994) Microalgae: Biotechnology and microbiology. Cambridge University Press, CambridgeGoogle Scholar
  10. Bellou S, Aggelis G (2013) Biochemical activities in Chlorella sp. and Nannochloropsis salina during lipid and sugar synthesis in a lab-scale open pond simulating reactor. J Biotechnol 164:318–329CrossRefGoogle Scholar
  11. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493PubMedCrossRefGoogle Scholar
  12. Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A, Cohen Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 5:497–503CrossRefGoogle Scholar
  13. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  14. Botes L, Price B, Waldron M, Pitcher GC (2002) A simple and rapid scanning electron microscope preparative technique for delicate “gymnodinioid” dinoflagellates. Microsc Res Tech 59:128–130PubMedCrossRefGoogle Scholar
  15. Boussiba S, Vonshak A, Cohen Z, Avissar Y, Richmond A (1987) Lipid and biomass production by the halotolerant microalga Nannochloropsis salina. Biomass 12:37–47CrossRefGoogle Scholar
  16. Bromke MA, Sabir JS, Alfassi FA, Hajarah NH, Kabli SA, Al-Malki AL, Ashworth MP, Méret M, Jansen RK, Willmitzer L (2015) Metabolomic profiling of 13 diatom cultures and their adaptation to nitrate-limited growth conditions. PLoS One 10(10):e0138965PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brown MR (2002) Nutritional value of microalgae for aquaculture. In: Cruz-Suárez LE, Ricque-Marie D, Tapia Salazar M, Gaxiola-Cortés MG, Simoes N (eds) Avances en NutriciónAcuícola VI. Memorias del VI Simposium Internacional de Nutrición Acuícola Cancún, Quintana Roo, México, pp 281–292Google Scholar
  18. Bruder K, Medlin LK (2007) Molecular assessment of phylogenetic relationships in selected species/genera in the naviculoid diatoms (bacillariophyta) the genus Placoneis. Nova Hedwigia 85:331–352CrossRefGoogle Scholar
  19. Caudales R, Wells JM, Butterfield JE (2000) Cellular fatty acid composition of cyanobacteria. II. Order Pleurocapsales. Int J Syst Evol Microbiol 50:1029–1034PubMedCrossRefGoogle Scholar
  20. Chaundhary R, Khattar JIS, Singh DP (2014) Microalgae as feedstock for biofuel: Biomass yield, lipid content and fatty acid composition as selection criteria. IJPRES 1:62–71Google Scholar
  21. Chaung K-C, Chu C-Y, Su Y-M, Chen Y-M (2012) Effect of culture conditions on growth, lipid content, and fatty acid composition of Aurantiochytrium mangrovei strain BL10. AMB Express 2:42PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chen YC (2012) The biomass and total lipid content and composition of twelve species of marine diatoms cultured under various environments. Food Chem 131:211–219CrossRefGoogle Scholar
  23. Chen W, Zhang C, Song L, Sommerfeld M, Hu Q (2009) A high throughput nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 77:41–47PubMedCrossRefGoogle Scholar
  24. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306PubMedCrossRefGoogle Scholar
  25. Christophe G, Kumar V, Nouaille R, Gaudet G, Fontanille P, Pandey A, Soccol CR, Larroche C (2012) Recent developments in microbial oils production: A possible alternative to vegetable oils for biodiesel without competition with human food? Braz Arch Biol Technol 55:29–46CrossRefGoogle Scholar
  26. Chtourou H, Dahmen I, Jebali A, Karray F, Hassairi I, Abdelkafi S, Ayadi H, Sayadi S, Dhouib A (2015) Characterization of Amphora sp., a newly isolated diatom wild strain, potentially usable for biodiesel production. Bioprocess Biosyst Eng 38:1381–1392PubMedCrossRefGoogle Scholar
  27. Cicci A, Bravi M (2016) Fatty acid composition and technological quality of the lipids produced by the microalga Scenedesmus dimorphus 1237 as a function of culturing conditions. Chem Eng Trans 49:181–186Google Scholar
  28. Csavina JL, Stuart BJ, Riefler RG, Vis ML (2011) Growth optimization of algae for biodiesel production. J Appl Microbiol 111:312–318PubMedCrossRefGoogle Scholar
  29. Damiani MC, Popovich CA, Constenla D, Leonardo PI (2010) Lipid analysis in Haematococcus pluvialis to assess its potential use as a biodiesel feedstock. Bioresour Technol 101:3801–3807PubMedCrossRefGoogle Scholar
  30. Dams E, Hendriks L, Van de Peer Y, Neefs JM, Smits G, Vandenbempt I, De Wachter R (1988) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 16:87–173CrossRefGoogle Scholar
  31. de la Vega M, Díaz E, Vila M, León R (2011) Isolation of a new strain of Picochlorum sp and characterization of its potential biotechnological applications. Biotechnol Prog 27:1535–1543PubMedCrossRefGoogle Scholar
  32. del Campo EM, del Hoyo A, Royo C, Casano LM, Álvarez R, Barreno E (2010) A single primer pair gives a specific ortholog amplicon in a wide range of cyanobacteria and plastid-bearing organisms: Applicability in inventory of reference material from collections and phylogenetic analysis. Mol Phylogenet Evol 57:1323–1328PubMedCrossRefGoogle Scholar
  33. Demirbas A (1998) Fuel properties and calculation of higher heating values of vegetable oils. Fuel 77:1117–1120CrossRefGoogle Scholar
  34. Demirbas A (2007) Importance of biodiesel as transportation fuel. Energ Policy 35:4661–4670CrossRefGoogle Scholar
  35. Demirbas A (2009) Global renewable energy projections. Energ Source Part B 4:212–224CrossRefGoogle Scholar
  36. Doucha J, Livansky K (2006) Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a middle and southern European climate. J Appl Phycol 18:811–826CrossRefGoogle Scholar
  37. Du W, Li W, Sun T, Chen X, Liu D (2008) Perspectives for biotechnological production of biodiesel and impacts. Appl Microbiol Biotechnol 79:331–337PubMedCrossRefGoogle Scholar
  38. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  39. Dunn RO (2011) Improving the cold flow properties of biodiesel by fractionation. In: Tzi-Bun N (ed) Soybean-applications and technology. InTech Open Access Publisher, Rijeka, pp 211–240Google Scholar
  40. Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. J Exp Mar Biol Ecol 161:115–134CrossRefGoogle Scholar
  41. Dunstan GA, Volkman JK, Barrett SM, Leroi J-M, Jeffrey SW (1993) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155–161CrossRefGoogle Scholar
  42. Eizadora TY, Zendejas FJ, Lane PD, Gaucher S, Simmons BA, Lane TW (2009) Triacylglycerol accumulation and profiling in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (bacillariophyceae) during starvation. J Appl Phycol 21:669–681CrossRefGoogle Scholar
  43. El-Kassas HY (2013) Growth and fatty acid profile of the marine microalga Picochlorum sp. grown under nutrient stress conditions. Egypt J Aquat Res 39:233–239CrossRefGoogle Scholar
  44. Elsey D, Jameson D, Raleigh B, Cooney MJ (2007) Fluorescent measurement of microalgal neutral lipids. J Microbiol Methods 68:639–642PubMedCrossRefGoogle Scholar
  45. Ferrer C, Colom F, Frasés S, Mulet E, Abad JL, Alio JL (2001) Detection and identification of fungal pathogens by PCR and by ITS2 and 5.8S ribosomal DNA typing in ocular infections. J Clin Microbiol 39:2873–2879PubMedPubMedCentralCrossRefGoogle Scholar
  46. Fidalgo JP, Cid A, Torres E, Sukenik A, Herrero C (1998) Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture 166:105–116CrossRefGoogle Scholar
  47. Fucikova K, Leliaert F, Cooper ED, Skaloud P, D’Hondt S, De Clerck O, Gurgel F, Lewis LA, Lewis PO, Lopez-Bautista J, Delwiche CF, Verbruggen H (2014) New phylogenetic hypotheses for the core Chlorophyta based on chloroplast sequence data. Front Ecol Evol 2:63Google Scholar
  48. Furnas MJ (1990) In situ growth rates of marine phytoplankton - approaches to measurement, community and species growth rates. J Plankton Res 12:1117–1151CrossRefGoogle Scholar
  49. Grant E (2008) Handbook of phycological methods: Developmental and cytological methods. Cambridge University Press, CambridgeGoogle Scholar
  50. Greenspan P, Mayer EP, Fowler SD (1985) Nile red: A selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100:965–973PubMedCrossRefGoogle Scholar
  51. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507CrossRefGoogle Scholar
  52. Grima ME, Medina RA, Giménez GA, Pérez SJA, Camacho GF, Sánchez GJL (1994) Comparison between extraction of lipids and fatty acids from microalgal biomass. J Am Oil Chem Soc 71:955–959CrossRefGoogle Scholar
  53. Guillard RRL (1973) Division rates. In: Stein JR (ed) Handbook of phycological methods, vol 1. Cambridge University Press, Cambridge, pp 289–312Google Scholar
  54. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60Google Scholar
  55. Hamilton ML, Warwick J, Terry A, Allen MJ, Napier JA, Sayanova O (2015) Towards the industrial production of omega-3 long chain polyunsaturated fatty acids from a genetically modified diatom Phaeodactylum tricornutum. PLoS One 10:e0144054PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hamsher SE, Evans KM, Mann DG, Poulickova A, Saunders GW (2011) Barcoding diatoms: Exploring alternatives to COI-5P. Protist 162:405–422PubMedCrossRefGoogle Scholar
  57. Higgins BT, Nobles D, Ma Y, Wikoff W, Kind T, Fiehn O, Brand J, VanderGheynst JS (2015) Informatics for improved algal taxonomic classification and research: A case study of UTEX 2341. Algal Res 12:545–549Google Scholar
  58. Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R (2012) The place of diatoms in the biofuel industry. Biofuels 3:221–240Google Scholar
  59. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: Perspectives and advances. Plant J 54:621–639PubMedCrossRefGoogle Scholar
  60. Huntley ME, Johnson ZI, Brown SL, Sills DL, Gerber L, Archibald I, Machesky SC, Granados J, Beal C, Greene CH (2015) Demonstrated large-scale production of marine microalgae for fuels and feed. Algal Res 10:249–265CrossRefGoogle Scholar
  61. Hytonen E, Jussila A, Kuusikunnas S (2014) Algal energy roadmap in India: Opportunities for Finnish industries and SMEs. VTT Technology, EspooGoogle Scholar
  62. Islam MA, Magnusson M, Brown RJ, Ayoko GA, Nabi MN, Heimann K (2013) Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles. Energies 6:5676–5702CrossRefGoogle Scholar
  63. Jiang Y, Yoshida T, Quigg A (2012) Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiol Biochem 54:70–77PubMedCrossRefGoogle Scholar
  64. Joseph MM, Renjith KR, John G, Nair SM, Chandramohanakumar N (2016) Biodiesel prospective of five diatom strains using growth parameters and fatty acid profiles. Biofuels 8:81–89Google Scholar
  65. Joseph KJ, Saramma AV (2011) Marine benthic microalgae of India: A monograph. St. Francis Press, KochiGoogle Scholar
  66. Kazuhisa M (ed)(1997) Microalgae as biological sources of lipids and hydrocarbons. In: Renewable biological systems for alternative sustainable energy production. Food and Agricultural Organization of the United Nations. Bulletin128. Osaka, Japan, pp 82–83Google Scholar
  67. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638CrossRefGoogle Scholar
  68. Knothe G (2006) Analyzing biodiesel: Standards and other methods. J Am Oil Chem Soc 83:823–833CrossRefGoogle Scholar
  69. Knothe G (2008) “Designer” biodiesel: optimizing fatty ester composition to improve fuel properties. Energy Fuel 22:1358–1364CrossRefGoogle Scholar
  70. Knothe G (2009) Improving biodiesel fuel properties by modifying fatty ester composition. Energy Environ Sci 2:759–766CrossRefGoogle Scholar
  71. Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution in microalgae: A comprehensive analysis of more than 2000strains from the SAG culture collection. BMC Plant Biol 11:124PubMedPubMedCentralCrossRefGoogle Scholar
  72. Lei A, Chen H, Shen G, Hu Z, Chen L, Wang J (2012) Expression of fatty acid synthesis genes and fatty acid accumulation in Haematococcus pluvialis under different stressors. Biotechnol Biofuels 5:18PubMedPubMedCentralCrossRefGoogle Scholar
  73. Lemieux C, Otis C, Turmel M (2014) Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae. BMC Evol Biol 14:211PubMedPubMedCentralCrossRefGoogle Scholar
  74. Li Y, Du W (2013) Effect of phospholipids on free lipase mediated methanolysis for biodiesel production. J Mol Catal B Enzym 91:67–71CrossRefGoogle Scholar
  75. Liang Y, Mai K (2005) Effect of growth phase on the fatty acid compositions of four species of marine diatoms. J Ocean Univ China 4:157–162CrossRefGoogle Scholar
  76. Liang Y, Maeda Y, Sunaga Y, Muto M, Matsumoto M, Yoshino T, Tanaka T (2013) Biosynthesis of polyunsaturated fatty acids in the oleaginous marine diatom Fistulifera sp. strain JPCC DA0580. Mar Drugs 11:5008–5023PubMedPubMedCentralCrossRefGoogle Scholar
  77. Liang Y, Maeda Y, Yoshino T, Matsumoto M, Tanaka T (2014) Profiling of fatty acid methyl esters from the oleaginous diatom Fistulifera sp. strain JPCC DA0580 under nutrition-sufficient and-deficient conditions. J Appl Phycol 26:2295–2302CrossRefGoogle Scholar
  78. Lim DKY, Garg S, Timmins M, Zhang ESB, Thomas-Hall SR, Schuhmann H, Li Y, Schenk PM (2012) Isolation and evaluation of oil-producing microalgae from subtropical coastal and brackish waters. PLoS One 7:e40751PubMedPubMedCentralCrossRefGoogle Scholar
  79. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  80. Lum KK, Kim J, Lei XG (2013) Dual potential of microalgae as a sustainable biofuel feedstock and animal feed. J Anim Sci Biotechnol 4:53PubMedPubMedCentralCrossRefGoogle Scholar
  81. Makri A, Bellou S, Birkou M, Papatrehas K, Dolapsakis NP, Bokas D, Papanikolaou S, Aggelis G (2011) Lipid synthesized by microalgae grown in laboratory and industrial scale bioreactors. Eng Life Sci 11:52–58CrossRefGoogle Scholar
  82. Markou G, Nerantzis E (2013) Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions. Biotechnol Adv 31:1532–1542PubMedCrossRefGoogle Scholar
  83. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: A review. Renew Sust Energ Rev 14:217–232CrossRefGoogle Scholar
  84. Matsumoto M, Sugiyama H (2010) Marine diatom, Navicula sp. strain JPCC DA0580 and marine green alga, Chlorella sp. strain NKG400014 as potential sources for biodiesel production. Appl Biochem Biotechnol 161:483–490PubMedCrossRefGoogle Scholar
  85. Mittelbach M, Remschmidt C (2004) Biodiesel: the comprehensive handbook. Boersedruck Ges. MBH, ViennaGoogle Scholar
  86. Mohammady NG (2011) Characterization of the fatty acid composition of Nannochloropsis salina as a determinant of biodiesel properties. Z Naturforsch C 66:328–332PubMedCrossRefGoogle Scholar
  87. Moro CV, Crouzet O, Thouvenot A, Batisson I, Bohatier J (2009) New design strategy for development of specific primer sets for PCR-based detection of chlorophyceae and bacillariophyceae in environmental sample. Appl Environ Microbiol 75:5729–5733PubMedCrossRefGoogle Scholar
  88. Mutanda T, Ramesh D, Karthikeyan S, Kumari S, Anandraj A, Bux F (2011) Bioprospecting for hyper-lipid producing microalgal strains for sustainable biofuel production. Bioresour Technol 102:57–70PubMedCrossRefGoogle Scholar
  89. Nascimento IA, Marques SSI, Cabanelas ITD, Pereira SA, Druzian JI, de Souza CO, Vich DV, de Carvalho GC, Nascimento MA (2013) Screening microalgae strains for biodiesel production: Lipid productivity and estimation of fuel quality based on fatty acids profiles as selective criteria. Bioenerg Res 6:1–13CrossRefGoogle Scholar
  90. Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ (2007) Vertical distribution of picoeukaryotic diversity in the open ocean. Environ Microbiol 9:1233–1252PubMedCrossRefGoogle Scholar
  91. Patil V, Kallqvist T, Olsen E, Vogt G, Gislerod HR (2007) Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquac Int 15:1–9CrossRefGoogle Scholar
  92. Pekarkova B, Hindak F, Šmarda J (1988) Morphological characteristics and physiological properties of a coccoid rhodophycean alga Rhodella grisea from thermal springs at Pieštny, Czechoslovakia. Arch Protistenkd 135:69–83CrossRefGoogle Scholar
  93. Pereira H, Barreira L, Mozes A, Florindom C, Polo C, Duarte CV, Varela J (2011) Microplate based high throughput screening procedure for the isolation of lipid-rich marine microalgae. Biotechnol Biofuels 4:1–12CrossRefGoogle Scholar
  94. Popovich CA, Damiani C, Constenla D, Leonardi PI (2012) Lipid quality of the diatoms Skeletonema costatum and Navicula gregaria from the South Atlantic Coast (Argentina): Evaluation of its suitability as biodiesel feedstock. J Appl Phycol 24:1–10CrossRefGoogle Scholar
  95. Ramachandra TV, Mahapatra DM, Karthick B (2009) Milking diatoms for sustainable energy: Biochemical engineering versus gasoline-secreting diatom solar panels. Ind Eng Chem Res 48:8769–8788CrossRefGoogle Scholar
  96. Ratledge C, Cohen Z (2008) Microbial and algal lipids: Do they have a future for biodiesel or as commodity oils? Lipid Technol 20:155–160CrossRefGoogle Scholar
  97. Recht L, Zarka A, Boussiba S (2012) Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl Microbiol Biotechnol 94:1495–1503PubMedCrossRefGoogle Scholar
  98. Renaud SM, Thinh LV, Parry DL (1999) The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170:147–159CrossRefGoogle Scholar
  99. Rodolfi L, Zittelli CG, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112PubMedCrossRefGoogle Scholar
  100. Ryckebosch E, Bruneel C, Termote-Verhalle R, Goiris K, Muylaert K, Foubert I (2014) Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative to fish oil. Food Chem 160:393–400PubMedCrossRefGoogle Scholar
  101. Schenk P, Thomas-Hall S, Stephens E, Marx U, Mussgnug J, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: High efficiency microalgae for biodiesel production. Bioenerg Res 1:20–43CrossRefGoogle Scholar
  102. Schindler J, Zittel W (2008) Crude Oil – The supply outlook. 102. Energy Watch Group, Ottoburnn, pp 1–102Google Scholar
  103. Schneiter R, Daum G (2006) Analysis of yeast lipids. In: Xiao W (ed) Yeast protocols: Methods in molecular biology, vol 313, 2nd edn. Humana Press, Totowa, pp 75–84Google Scholar
  104. 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 25:453–465CrossRefGoogle Scholar
  105. Senapin S, Phiwsaiya K, Kiatmetha P, Withyachumnarnkul B (2011) Development of primers and a procedure for specific identification of the diatom Thalassiosira weissflogii. Aquac Int 19:693–704CrossRefGoogle Scholar
  106. Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisso F, Triantaphylidès C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: Characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sivakumar G, Vail DR, Xu J, Burner DM, Lay JO, Ge X, Weathers PJ (2010) Bioethanol and biodiesel: Alternative liquid fuels for future generations. Eng Life Sci 10:8–18CrossRefGoogle Scholar
  108. Stansell GR, Gray VM, Stuart DS (2012) Microalgal fatty acid composition: Implications for biodiesel quality. J Appl Phycol 24:791–801CrossRefGoogle Scholar
  109. Stephens E, Ross IL, Hankamer B (2013) Expanding the microalgal industry-continuing controversy or compelling case? Curr Opin Chem Biol 17:444–452PubMedCrossRefGoogle Scholar
  110. Talebi AF, Tabatabaei M, Chisti Y (2014) Biodiesel analyzer: An user-friendly software for predicting the properties of prospective biodiesel. Biofuel Res J 2:55–57CrossRefGoogle Scholar
  111. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedPubMedCentralCrossRefGoogle Scholar
  112. Thomas CR (1997) Identifying marine phytoplankton. Academic Press, CaliforniaGoogle Scholar
  113. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: The sensitivity of progressive multiple sequence alignment through sequence weighting, position- specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedPubMedCentralCrossRefGoogle Scholar
  114. Tonon T, Harvey D, Larson TR, Graham IA (2002) Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61:15–24PubMedCrossRefGoogle Scholar
  115. Viso AC, Marty JC (1993) Fatty acids from 28 marine microalgae. Phytochemistry 34:1521–1533CrossRefGoogle Scholar
  116. Volkman JK, Dunstan GA, Jeffrey SW, Kearney PS (1991) Fatty acids from microalgae of the genus Pavlova. Phytochemistry 30:1855–1859CrossRefGoogle Scholar
  117. Volkman JK, Eglinton G, Corner EDS (1980) Sterols and fatty acids of marine diatom Biddulphia sinensis. Phytochemistry 19:1809–1813CrossRefGoogle Scholar
  118. Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J Exp Mar Biol Ecol 128:219–240CrossRefGoogle Scholar
  119. Walne PR (1970) Studies on the food value of nineteen genera of algae to juvenile bivalves of the genera Ostrea, Crassostrea, Mercenaria and Mytilis. Fish Investig 26:1–62Google Scholar
  120. Williams PJLB, Laurens LML (2010) Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics. Energy Environ Sci 3:554–590CrossRefGoogle Scholar
  121. Wishart DS, Stothard P, Van Domselaar GH (2000) PepTool™ and GeneTool™: Platform-independent tools for biological sequence analysis. Methods Mol Biol 132:93–113PubMedGoogle Scholar
  122. Wu X, Zarka A, Boussiba S (2000) A simplified protocol for preparing DNA from filamentous cyanobacteria. Plant Mol Biol Report 18:385–339CrossRefGoogle Scholar
  123. Xu H, Miao X, Wu Q (2006) High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. J Biotechnol 126:499–507PubMedCrossRefGoogle Scholar
  124. Zhang Q, Hong Y (2014) Effects of stationary phase elongation and initial nitrogen and phosphorus concentrations on the growth and lipid-producing potential of Chlorella sp. HQ. J Appl Phycol 26:141–149CrossRefGoogle Scholar
  125. Zhu LD, Hiltunen E, Antila E, Zhong JJ, Yuan ZH, Wang ZM (2014) Microalgal biofuels: Flexible bioenergies for sustainable development. Renew Sust Energ Rev 30:1035–1046CrossRefGoogle Scholar
  126. Zhu L, Ketola T (2012) Microalgae production as a biofuel feedstock: Risks and challenges. Int J Sust Dev World 19:268–274Google Scholar
  127. Zhu CJ, Lee YK, Chao TM (1997) Effects of temperature and growth phase on lipid and biochemical composition Isochrysis galbana TK1. J Appl Phycol 9:451–457CrossRefGoogle Scholar
  128. Zhukova NV, Aizdaicher NA (1995) Fatty acid composition of 15 species of marine microalgae. Phytochemistry 39(2):351–356Google Scholar
  129. Zimmermann J, Jahn R, Gemeinholzer B (2011) Barcoding diatoms: Evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Org Divers Evol 1:173CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Sanyo Sabu
    • 1
  • I.S. Bright Singh
    • 1
  • Valsamma Joseph
    • 1
    Email author
  1. 1.National Centre for Aquatic Animal HealthCochin University of Science and TechnologyKochiIndia

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