Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Screening of High Temperature-Tolerant Oleaginous Diatoms

  • Zhang, Lingxiang (Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences) ;
  • Hu, Fan (School of Foreign Languages, China University of Geosciences) ;
  • Wan, Xiu (Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences) ;
  • Pan, Yufang (Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences) ;
  • Hu, Hanhua (Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences)
  • Received : 2020.02.27
  • Accepted : 2020.04.20
  • Published : 2020.07.28
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Abstract

Screening suitable strains with high temperature adaptability is of great importance for reducing the cost of temperature control in microalgae cultivation, especially in summer. To obtain high temperature-tolerant diatoms, water samples were collected in summer from 7 different regions of China across the Northeast, North and East. A total of 731 water samples was collected and from them 131 diatom strains were isolated and identified based on the 18S rRNA sequences. Forty-nine strains out of the 131 diatoms could survive at 30℃, and 6 strains with relatively high biomass and lipid content at high temperature were selected and were found to be able to grow at 35℃. Cyclotella sp. HB162 had the highest dry biomass of 0.46 g/l and relatively high triacylglycerol (TAG) content of 237.4 mg/g dry biomass. The highest TAG content of 246.4 mg/g dry biomass was obtained in Fistulifera sp. HB236, while Nitzschia palea HB170 had high dry biomass (0.33 g/l) but relatively low TAG content (105.9 mg/g dry biomass). N. palea HB170 and Fistulifera sp. HB236 presented relatively stable growth rates and lipid yields under fluctuating temperatures ranging from 28 to 35℃, while Cyclotella HB162 maintained high lipid yield at temperatures below 25℃. The percentage of saturated fatty acids and monounsaturated fatty acids in all the 6 strains was 84-91% in total lipids and 90-94% in TAGs, which makes them the ideal feedstock for biodiesel.

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References

  1. Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, et al. 2008. Second generation biofuels: high-efficiency microalgae for biodiesel production. BioEnergy Res. 1: 20-43. https://doi.org/10.1007/s12155-008-9008-8
  2. Meng X, Yang J, Xu X, Zhang L, Nie Q, Xian M. 2009. Biodesel production from oleaginous microorganisms. Renew. Energy. 34: 1-5. https://doi.org/10.1016/j.renene.2008.04.014
  3. Mata TM, Martins AA, Caetano NS. 2010. Microalgae for biodiesel production and other applications: a review. Renew. Sust. Energ. Rev. 14: 217-232. https://doi.org/10.1016/j.rser.2009.07.020
  4. Chisti Y. 2019. Introduction to algal fuels, pp. 1-31. In Pandey A, Chang JS, Soccol CR, Lee DJ, Chisti Y (eds.), pp. 603. Biofuels from Algae (2nd Edition). Elsevier, Boston, MA, USA.
  5. Borowitzka MA, Moheimani NR. 2013. Sustainable biofuels from algae. Mitig. Adapt. Strat. Gl. 18: 13-25. https://doi.org/10.1007/s11027-010-9271-9
  6. Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, et al. 2009. Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol. Bioeng. 102: 100-112. https://doi.org/10.1002/bit.22033
  7. Wijffels RH, Barbosa MJ. 2010. An outlook on microalgal biofuels. Science 329: 796-799. https://doi.org/10.1126/science.1189003
  8. Chen X, He G, Deng Z, Wang N, Jiang W, Chen S. 2014. Screening of microalgae for biodiesel feedstock. Adv. Microbiol. 4: 365-376. https://doi.org/10.4236/aim.2014.47044
  9. Gao C, Zhai Y, Ding Y, Wu Q. 2010. Application of sweet sorghum for biodiesel production by heterotrophic microalga Chlorella protothecoides. Appl. Energy 87: 756-761. https://doi.org/10.1016/j.apenergy.2009.09.006
  10. Lam MK, Lee KT. 2012. Potential of using organic fertilizer to cultivate Chlorella vulgaris for biodiesel production. Appl. Energy 94: 303-308. https://doi.org/10.1016/j.apenergy.2012.01.075
  11. Vooren GV, Grand FL, Legrand J, Cuine S, Peltiere G, Pruvost J. 2012. Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresour. Technol. 124: 421-432. https://doi.org/10.1016/j.biortech.2012.08.009
  12. Traller JC, Cokus SJ, Lopez DA, Gaidarenko O, Smith SR, McCrow JP, et al. 2016. Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype. Biotechnol. Biofuels 9: 258. https://doi.org/10.1186/s13068-016-0670-3
  13. Yu S-J, Shen X-F, Ge H-Q, Zheng H, Chu F-F, Hu H, et al. 2016. Role of sufficient phosphorus in biodiesel production from diatom Phaeodactylum tricornutum. Appl. Microbiol. Biotechnol. 100: 6927-6934. https://doi.org/10.1007/s00253-016-7641-2
  14. Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R. 2012. The place of diatoms in the biofuels industry. Biofuels 3: 221-240. https://doi.org/10.4155/bfs.11.157
  15. Kooistra WHCF, Gersonde R, Medlin LK, Mann DG. 2007. The origin and evolution of the diatoms: their adaptation to a planktonic existence, pp. 207-249. In Falkowski PG, Knoll AH (eds.), Evolution of primary producers in the sea. Elsevier, Boston, MA, USA.
  16. Rousch JM, Bingham SE, Sommerfeld MR. 2003. Changes in fatty acid profiles of thermo-intolerant and thermo-tolerant marine diatoms during temperature stress. J. Exp. Mar. Biol. Ecol. 295: 145-156. https://doi.org/10.1016/S0022-0981(03)00293-4
  17. Hu H, Gao K. 2006. Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated $CO_2$ concentration. Biotechnol. Lett. 28: 987-992. https://doi.org/10.1007/s10529-006-9026-6
  18. 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: 5676-5702. https://doi.org/10.3390/en6115676
  19. Singh DK, Mallick N. 2014. Accumulation potential of lipids and analysis of fatty acid profile of few microalgal species for biodiesel feedstock. J. Microbiol Biotechnol. Res. 4: 37-44.
  20. Lebeau T, Robert JM. 2003. Diatom cultivation and biotechnologically relevant products. Part I: cultivation at various scales. Appl. Microbiol. Biotechnol. 60: 612-623. https://doi.org/10.1007/s00253-002-1176-4
  21. Xu J, Hu H. 2013. Screening high oleaginous Chlorella strains from different climate zones. Bioresour. Technol. 144: 637-643. https://doi.org/10.1016/j.biortech.2013.07.029
  22. Otsuki A, Watanabe M M, Sugahara K. 1987. Chlorophyll pigments in methanol extracts from ten axenic cultured diatoms and three green algae as determined by reverse phase HPLC with fluorometric detection. J. Phycol. 23: 406-414. https://doi.org/10.1111/j.1529-8817.1987.tb02526.x
  23. Hu H, Li H, Xu X. 2008. Alternative cold response modes in Chlorella (Chlorophyta, Trebouxiophyceae) from Antarctica. Phycologia 47: 28-34. https://doi.org/10.2216/07-28.1
  24. Swofford DL. 1998. PAUP* 4.0-phylogenetic analysis using parsimony (*and other methods). pp. 604. Sinauer Associates, Sunderland.
  25. Reiser S, Somerville C. 1997. Isolation of mutants of Acinetobacter calcoaceticus deficient in wax ester synthesis and complementation of one mutation with a gene encoding a fatty acyl-coenzyme a reductase. J. Bacteriol. 179: 2969-2975. https://doi.org/10.1128/JB.179.9.2969-2975.1997
  26. Bligh EG, Dyer WJ. 1959. A rapid method of lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917. https://doi.org/10.1139/o59-099
  27. Willen E. 1991. Planktonic diatoms - an ecological review. Algol. Stud. 62: 69-106.
  28. Lundholm N, Daugbjerg N, Moestrup O. 2002. Phylogeny of the Bacillariaceae with emphasis on the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU rDNA. Eur. J. Phycol. 37: 115-134. https://doi.org/10.1017/S096702620100347X
  29. Hasle G R. 1994. Pseudo-Nitzschia as a genus distinct from Nitzschia (Bacillariophyceae). J. Phycol. 30: 1036-1039. https://doi.org/10.1111/j.0022-3646.1994.01036.x
  30. Tanaka T, Maeda Y, Veluchamy A, Tanaka M, Abida H, Marechal E, et al. 2015. Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell 27: 162-176. https://doi.org/10.1105/tpc.114.135194
  31. Potapova MG, Charles DF. 2002. Benthic diatoms in USA rivers: distributions along spatial and environmental gradients. J. Biogeogr. 29: 167-187. https://doi.org/10.1046/j.1365-2699.2002.00668.x
  32. Clement R, Jensen E, Prioretti L, Maberly SC, Gontero B. 2017. Diversity of $CO_2$-concentrating mechanisms and responses to $CO_2$ concentration in marine and freshwater diatoms. J. Exp. Bot. 68: 3925-3935. https://doi.org/10.1093/jxb/erx035
  33. Trobajo R, Clavero E, Chepurnov VA, Sabbe K, Mann DG, Ishihara S, et al. 2009. Morphological, genetic and mating diversity within the widespread bioindicator Nitzschia palea (Bacillariophyceae). Phycologia 48: 443-459. https://doi.org/10.2216/08-69.1
  34. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, et al. 2008. Microalgael triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54: 621-639. https://doi.org/10.1111/j.1365-313X.2008.03492.x
  35. Lavens P, Sorgeloos P. 1996. Manual on the production and use of live food for aquaculture. pp. 295. FAO Fisheries Technical Paper, Rome.
  36. Shafik HM, Herodek S, Voros L, Presing M, Kiss KT. 1997. Growth of Cyclotella meneghiniana Kutz. I. Effects of temperature, light and low rate of nutrient supply. Ann. Limnol.-Int. J. Lim. 33: 139-147. https://doi.org/10.1051/limn/1997014
  37. Li X, Marella TK, Tao L, Li R, Tiwari A, Li Gu. 2017. Optimization of growth conditions and fatty acid analysis for three freshwater diatom isolates. Phycol. Res. 65: 177-187. https://doi.org/10.1111/pre.12174
  38. Jiang Y, Laverty KS, Brown J, Nunez M, Brown L, Chagoya J, et al. 2014. Effects of fluctuating temperature and silicate supply on the growth, biochemical composition and lipid accumulation of Nitzschia sp. Bioresour. Technol. 154: 336-344. https://doi.org/10.1016/j.biortech.2013.12.068
  39. Sato R, Maeda Y, Yoshino T, Tanaka T, Matsumoto M. 2014. Seasonal variation of biomass and oil production of the oleaginous diatom Fistulifera sp. in outdoor vertical bubble column and raceway-type bioreactors. J. Biosci. Bioeng. 117: 720-724. https://doi.org/10.1016/j.jbiosc.2013.11.017
  40. European Standard EN. 2004. Automotive fuels-fatty acid methyl esters (FAME) for diesel engines-requirements and test methods. pp. 28. AFNOR, Saint-Denis.
  41. Renaud S, Zhou H, Parry D, Thinh L-V, Woo K. 1995. Effect of temperature on the growth, total lipid content and fatty acid composition of recently isolated tropical microalgae Isochrysis sp., Nitzschia closterium, Nitzschia paleacea, and commercial species Isochrysis sp. (clone T. ISO). J. Appl. Phycol. 7: 595-602. https://doi.org/10.1007/BF00003948
  42. Jiang H, Gao K. 2004. Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J. Phycol. 40: 651-654. https://doi.org/10.1111/j.1529-8817.2004.03112.x
  43. Teoh M-L, Phang S-M, Chu W-L. 2013. Response of Antarctic, temperate, and tropical microalgae to temperature stress. J. Appl. Phycol. 25: 285-297. https://doi.org/10.1007/s10811-012-9863-8
  44. Pasquet V, Ulmann L, Mimouni V, Guiheneuf F, Jacquette B, Morant-Manceau A, et al. 2014. Fatty acids profile and temperature in the cultured marine diatom Odontella aurita. J. Appl. Phycol. 26: 2265-2271. https://doi.org/10.1007/s10811-014-0252-3
  45. Schaub I, Wagner H, Graeve M, Karsten U. 2017. Effects of prolonged darkness and temperature on the lipid metabolism in the benthic diatom Navicula perminuta from the Arctic Adventfjorden, Svalbard. Polar Biol. 40: 1425-1439. https://doi.org/10.1007/s00300-016-2067-y
  46. Svenning JB, Dalheim L, Eilertsen HC, Vasskog T. 2019. Temperature dependent growth rate, lipid content and fatty acid composition of the marine cold-water diatom Porosira glacialis. Algal Res. 37: 11-16. https://doi.org/10.1016/j.algal.2018.10.009
  47. Indrayani I, Moheimani NR, de Boer K, Bahri PA, Borowitzka MA. 2020. Temperature and salinity effects on growth and fatty acid composition of a halophilic diatom, Amphora sp. MUR258 (Bacillariophyceae). J. Appl. Phycol. 32: 977-987. https://doi.org/10.1007/s10811-020-02053-z