Effects of light and nitrogen availability on photosynthetic efficiency and fatty acid content of three original benthic diatom strains


Autoři: Eva Cointet aff001;  Gaëtane Wielgosz-Collin aff001;  Gaël Bougaran aff002;  Vony Rabesaotra aff001;  Olivier Gonçalves aff003;  Vona Méléder aff001
Působiště autorů: Université de Nantes, Laboratoire Mer Molécules Santé, Nantes, France aff001;  PBA-IFREMER, Nantes, France aff002;  Université de Nantes, GEPEA, Saint-Nazaire, Nantes, France aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224701

Souhrn

Microalgal biotechnology has gained considerable importance in recent decades. Applications range from simple biomass production for food and animal feed to valuable products for fuel, pharmaceuticals, health, biomolecules and materials relevant to nanotechnology. There are few reports of the exploration of wider microalgae biodiversity in the literature on high value microalgal compounds, however, because it is believed that there is little to be gained in terms of biomass productivity by examining new strains. Still, without diversity, innovation in biotechnology applications is currently limited. Using microalgal diversity is a very promising way to match species and processes for a specific biotechnological application. In this context, three benthic marine diatom strains (Entomoneis paludosa NCC18.2, Nitzschia alexandrina NCC33, and Staurosira sp NCC182) were selected for their lipid production and growth capacities. Using PAM fluorometry and FTIR spectroscopy, this study investigated the impact of nitrogen repletion and depletion as well as light intensity (30, 100, and 400 μmol.photons.m-2.s-1) on their growth, photosynthetic performance and macromolecular content, with the aim of improving the quality of their lipid composition. Results suggest that under high light and nitrogen limitation, the photosynthetic machinery is negatively impacted, leading cells to reduce their growth and accumulate lipids and/or carbohydrates. However, increasing lipid content under stressful conditions does not increase the production of lipids of interest: PUFA, ARA and EPA production decreases. Culture conditions to optimize production of such fatty acids in these three original strains led to a balance between economic and ecophysiological constraints: low light and no nitrogen limitation led to better photosynthetic capacities associated with energy savings, and hence a more profitable approach.

Klíčová slova:

Carbohydrates – Diatoms – Fatty acids – Light – Lipids – Phosphates – Pigments – Photosynthetic efficiency


Zdroje

1. Renaud S.M., Thinh L.-V., Parry D.L., The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture, Aquaculture. 170 (1999) 147–159.

2. Dunstan G.A., Volkman J.K., Barrett S.M., Leroi J.-M., Jeffrey S.W., Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae), Phytochemistry. 35 (1993) 155–161. doi: 10.1016/S0031-9422(00)90525-9

3. Volkman J.K., Jeffrey S.W., Nichols P.D., Rogers G.I., Garland C.D., Fatty acid and lipid composition of 10 species of microalgae used in mariculture, J. Exp. Mar. Biol. Ecol. 128 (1989) 219–240. doi: 10.1016/0022-0981(89)90029-4

4. d’Ippolito G., Sardo A., Paris D., Vella F.M., Adelfi M.G., Botte P., Gallo C., Fontana A., Potential of lipid metabolism in marine diatoms for biofuel production, Biotechnol. Biofuels. 8 (2015) 28. doi: 10.1186/s13068-015-0212-4 25763104

5. Joseph M.M., Renjith K.R., John G., Nair S.M., Chandramohanakumar N., Biodiesel prospective of five diatom strains using growth parameters and fatty acid profiles, Biofuels. 8 (2017) 81–89. doi: 10.1080/17597269.2016.1204585

6. Cointet E., Wielgosz-Collin G., Méléder V., Gonçalves O., Lipids in benthic diatoms: A new suitable screening procedure, Algal Res. 39 (2019) 101425. doi: 10.1016/j.algal.2019.101425

7. Doan T.T.Y., Sivaloganathan B., Obbard J.P., Screening of marine microalgae for biodiesel feedstock, Biomass Bioenergy. 35 (2011) 2534–2544. doi: 10.1016/j.biombioe.2011.02.021

8. Zhao F., Liang J., Gao Y., Luo Q., Yu Y., Chen C., Sun L., Variations in the total lipid content and biological characteristics of diatom species for potential biodiesel production, Fundam Renew Energy Appl. 6 (2016) 22–26.

9. Pulz O., Gross W., Valuable products from biotechnology of microalgae, Appl. Microbiol. Biotechnol. 65 (2004) 635–648. doi: 10.1007/s00253-004-1647-x 15300417

10. F. Shahidi, C. Barrow, Marine nutraceuticals and functional foods, CRC Press, 2007.

11. Rodolfi L., Chini Zittelli G., Bassi N., Padovani G., Biondi N., Bonini G., Tredici M.R., Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor, Biotechnol. Bioeng. 102 (2009) 100–112. doi: 10.1002/bit.22033 18683258

12. Huete-Ortega M., Okurowska K., Kapoore R.V., Johnson M.P., Gilmour D.J., Vaidyanathan S., Effect of ammonium and high light intensity on the accumulation of lipids in Nannochloropsis oceanica (CCAP 849/10) and Phaeodactylum tricornutum (CCAP 1055/1), Biotechnol. Biofuels. 11 (2018) 60. doi: 10.1186/s13068-018-1061-8 29541157

13. Mortensen S.H., Børsheim K.Y., Rainuzzo J., Knutsen G., Fatty acid and elemental composition of the marine diatom Chaetoceros gracilis Schütt. Effects of silicate deprivation, temperature and light intensity, J. Exp. Mar. Biol. Ecol. 122 (1988) 173–185.

14. Roessler P.G., Effects of silicon deficiency on lipid composition and metabolism in the diatom Cyclotella cryptica 1, J. Phycol. 24 (1988) 394–400.

15. Shifrin N.S., Chisholm S.W., Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles 1, J. Phycol. 17 (1981) 374–384.

16. Gao Y., Yang M., Wang C., Nutrient deprivation enhances lipid content in marine microalgae, Bioresour. Technol. 147 (2013) 484–491. doi: 10.1016/j.biortech.2013.08.066 24012737

17. Yongmanitchai W., Ward O.P., Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions., Appl Env. Microbiol. 57 (1991) 419–425.

18. Dempster T.A., Sommerfeld M.R., Effects of environmental conditions on growth and lipid accumulation in Nitzschia communis (Bacillariophyceae), J. Phycol. 34 (1998) 712–721.

19. Schaub I., Wagner H., Graeve M., Karsten U., Effects of prolonged darkness and temperature on the lipid metabolism in the benthic diatom Navicula perminuta from the Arctic Adventfjorden, Svalbard, Polar Biol. (2017) 1–15. doi: 10.1007/s00300-016-2067-y

20. Sriharan S., Sriharan T., Effects of nutrients and temperature on lipid and fatty acid production in the diatom Hantzshia DI-60, Appl. Biochem. Biotechnol. 24 (1990) 309.

21. Brown M.R., Dunstan G.A., Norwood S.J., Miller K.A., Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana 1, J. Phycol. 32 (1996) 64–73.

22. Spolaore P., Joannis-Cassan C., Duran E., Isambert A., Commercial applications of microalgae, J. Biosci. Bioeng. 101 (2006) 87–96. doi: 10.1263/jbb.101.87 16569602

23. Bondioli P., Della Bella L., Rivolta G., Zittelli G.C., Bassi N., Rodolfi L., Casini D., Prussi M., Chiaramonti D., Tredici M.R., Oil production by the marine microalgae Nannochloropsis sp. F&M-M24 and Tetraselmis suecica F&M-M33, Bioresour. Technol. 114 (2012) 567–572. doi: 10.1016/j.biortech.2012.02.123 22459965

24. Converti A., Casazza A.A., Ortiz E.Y., Perego P., Del Borghi M., Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production, Chem. Eng. Process. Process Intensif. 48 (2009) 1146–1151. doi: 10.1016/j.cep.2009.03.006

25. Liu Z.-Y., Wang G.-C., Zhou B.-C., Effect of iron on growth and lipid accumulation in Chlorella vulgaris, Bioresour. Technol. 99 (2008) 4717–4722. doi: 10.1016/j.biortech.2007.09.073 17993270

26. Roleda M.Y., Slocombe S.P., Leakey R.J.G., Day J.G., Bell E.M., Stanley M.S., Effects of temperature and nutrient regimes on biomass and lipid production by six oleaginous microalgae in batch culture employing a two-phase cultivation strategy, Bioresour. Technol. 129 (2013) 439–449. doi: 10.1016/j.biortech.2012.11.043 23262022

27. Chen Y.-C., The biomass and total lipid content and composition of twelve species of marine diatoms cultured under various environments, Food Chem. 131 (2012) 211–219. doi: 10.1016/j.foodchem.2011.08.062

28. Chuecas L., Riley J.P., Component fatty acids of the total lipids of some marine phytoplankton, J. Mar. Biol. Assoc. U. K. 49 (1969) 97. doi: 10.1017/S0025315400046439

29. Berges J.A., Charlebois D.O., Mauzerall D.C., Falkowski P.G., Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae, Plant Physiol. 110 (1996) 689–696. doi: 10.1104/pp.110.2.689 12226211

30. Giordano M., Kansiz M., Heraud P., Beardall J., Wood B., McNaughton D., Fourier transform infrared spectroscopy as a novel tool to investigate changes in intracellular macromolecular pools in the marine microalga Chaetoceros muellerii (Bacillariophyceae), J. Phycol. 37 (2001) 271–279.

31. Hildebrand M., Davis A.K., Smith S.R., Traller J.C., Abbriano R., The place of diatoms in the biofuels industry, Biofuels. 3 (2012) 221–240. doi: 10.4155/bfs.11.157

32. Geider R.J., La Roche J., Greene R.M., Olaizola M., Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation 1, J. Phycol. 29 (1993) 755–766.

33. Berges J.A., Falkowski P.G., Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation, Limnol. Oceanogr. 43 (1998) 129–135.

34. Parkhill J., Maillet G., Cullen J.J., Fluorescence‐based maximal quantum yield for PSII as a diagnostic of nutrient stress, J. Phycol. 37 (2001) 517–529.

35. Vassiliev I.R., Prasil O., Wyman K.D., Kolber Z., Hanson A.K., Prentice J.E., Falkowski P.G., Inhibition of PS II photochemistry by PAR and UV radiation in natural phytoplankton communities, Photosynth. Res. 42 (1994) 51–64. doi: 10.1007/BF00019058 24307468

36. Quigg A., Beardall J., Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae, Plant Cell Environ. 26 (2003) 693–703.

37. Sunda W.G., Huntsman S.A., Relationships among photoperiod, carbon fixation, growth, chlorophyll a, and cellular iron and zinc in a coastal diatom, Limnol. Oceanogr. 49 (2004) 1742–1753. doi: 10.4319/lo.2004.49.5.1742

38. Dubinsky Z., Rotem J., Relations between algal populations and the pH of their media, Oecologia. 16 (1974) 53–60. doi: 10.1007/BF00345087 28308951

39. Ralph P.J., Gademann R., Rapid light curves: a powerful tool to assess photosynthetic activity, Aquat. Bot. 82 (2005) 222–237.

40. Ritchie R.J., Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents, Photosynth. Res. 89 (2006) 27–41. doi: 10.1007/s11120-006-9065-9 16763878

41. Bligh E.G., Dyer W.J., A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol. 37 (1959) 911–917. doi: 10.1139/o59-099 13671378

42. Bougaran G., Bernard O., Sciandra A., Modeling continuous cultures of microalgae colimited by nitrogen and phosphorus, J. Theor. Biol. 265 (2010) 443–454. doi: 10.1016/j.jtbi.2010.04.018 20433853

43. Hansen H.P., Koroleff F., Determination of nutrients, Methods Seawater Anal. (1999) 159–228.

44. Amin S.A., Hmelo L.R., van Tol H.M., Durham B.P., Carlson L.T., Heal K.R., Morales R.L., Berthiaume C.T., Parker M.S., Djunaedi B., Ingalls A.E., Parsek M.R., Moran M.A., Armbrust E.V., Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria, Nature. 522 (2015) 98–101. doi: 10.1038/nature14488 26017307

45. Koroleff F., Direct determination of ammonia in natural waters as indophenol blue, Inf. Tech. Methods Seawater Anal. (1970) 19–22.

46. A. Aminot, R. Kérouel, Hydrologie des écosystèmes marins: paramètres et analyses, Editions Quae, 2004.

47. Beer S., Vilenkin B., Weil A., Veste M., Susel L., Eshel A., Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry, Mar. Ecol. Prog. Ser. 174 (1998) 293–300.

48. Eilers P., Peeters J., A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton, Ecol. Model. 42 (1988) 199–215.

49. Coat R., Montalescot V., León E.S., Kucma D., Perrier C., Jubeau S., Thouand G., Legrand J., Pruvost J., Gonçalves O., Unravelling the matrix effect of fresh sampled cells for in vivo unbiased FTIR determination of the absolute concentration of total lipid content of microalgae, Bioprocess Biosyst. Eng. 37 (2014) 2175–2187. doi: 10.1007/s00449-014-1194-5 24788985

50. León E.S., Coat R., Moutel B., Pruvost J., Legrand J., Gonçalves O., Influence of physical and chemical properties of HTSXT-FTIR samples on the quality of prediction models developed to determine absolute concentrations of total proteins, carbohydrates and triglycerides: a preliminary study on the determination of their absolute concentrations in fresh microalgal biomass, Bioprocess Biosyst. Eng. 37 (2014) 2371–2380. doi: 10.1007/s00449-014-1215-4 24861315

51. Brembu T., Mühlroth A., Alipanah L., Bones A.M., The effects of phosphorus limitation on carbon metabolism in diatoms, Philos. Trans. R. Soc. B Biol. Sci. 372 (2017) 20160406.

52. Bucciarelli E., Sunda W.G., Influence of CO2, nitrate, phosphate, and silicate limitation on intracellular dimethylsulfoniopropionate in batch cultures of the coastal diatom Thalassiosira pseudonana, Limnol. Oceanogr. 48 (2003) 2256–2265.

53. Brand L., Guillard R., The effects of continuous light and light intensity on the reproduction rates of twenty-two species of marine phytoplankton, J. Exp. Mar. Biol. Ecol. 50 (1981) 119–132.

54. Berges J.A., Franklin D.J., Harrison P.J., Evolution of an Artificial Seawater Medium: Improvements in Enriched Seawater, Artificial Water Over the Last Two Decades, J. Phycol. 37 (2001) 1138–1145. doi: 10.1046/j.1529-8817.2001.01052.x

55. McLachlan J., Some considerations of the growth of marine algae in artificial media, Can. J. Microbiol. 10 (1964) 769–782. doi: 10.1139/m64-098 14222659

56. Allen E.J., On the culture of the plankton diatom Thalassiosira grauida Cleve, in artificial sea-water, J. Mar. Biol. Assoc. U. K. 10 (1914) 417–439. doi: 10.1017/S0025315400008225

57. Guihéneuf F., Mimouni V., Ulmann L., Tremblin G., Environmental factors affecting growth and omega 3 fatty acid composition in Skeletonema costatum. The influences of irradiance and carbon source: Communication presented at the 25ème Congrès Annuel de l’Association des Diatomistes de Langue Francaise (ADLaF), Caen, 25–28 September 2006, Diatom Res. 23 (2008) 93–103.

58. He Q., Yang H., Wu L., Hu C., Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae, Bioresour. Technol. 191 (2015) 219–228. doi: 10.1016/j.biortech.2015.05.021 25997011

59. Norici A., Bazzoni A.M., Pugnetti A., Raven J.A., Giordano M., Impact of irradiance on the C allocation in the coastal marine diatom Skeletonema marinoi Sarno and Zingone*, Plant Cell Environ. 34 (2011) 1666–1677. doi: 10.1111/j.1365-3040.2011.02362.x 21707652

60. Rhee G.-‐ull, Gotham I.J., The effect of environmental factors on phytoplankton growth: Light and the interactions of light with nitrate limitation1, Limnol. Oceanogr. 26 (1981) 649–659. doi: 10.4319/lo.1981.26.4.0649

61. Solovchenko A.E., Khozin-Goldberg I., Didi-Cohen S., Cohen Z., Merzlyak M.N., Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa, J. Appl. Phycol. 20 (2008) 245–251. doi: 10.1007/s10811-007-9233-0

62. Jauffrais T., Drouet S., Turpin V., Méléder V., Jesus B., Cognie B., Raimbault P., Cosson R.P., Decottignies P., Martin-Jézéquel V., Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings, J. Exp. Mar. Biol. Ecol. 469 (2015) 83–92.

63. White S., Anandraj A., Bux F., PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids, Bioresour. Technol. 102 (2011) 1675–1682. doi: 10.1016/j.biortech.2010.09.097 20965719

64. Jiang Y., Yoshida T., Quigg A., Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae, Plant Physiol. Biochem. 54 (2012) 70–77. doi: 10.1016/j.plaphy.2012.02.012 22387274

65. Napoléon C., Raimbault V., Claquin P., Influence of nutrient stress on the relationships between PAM measurements and carbon Incorporation in four phytoplankton species, PLOS ONE. 8 (2013) e66423. doi: 10.1371/journal.pone.0066423 23805221

66. Wilhelm C., Jungandreas A., Jakob T., Goss R., Light acclimation in diatoms: From phenomenology to mechanisms, Mar. Genomics. 16 (2014) 5–15. doi: 10.1016/j.margen.2013.12.003 24412570

67. Anning T., MacIntyre H.L., Pratt S.M., Sammes P.J., Gibb S., Geider R.J., Photoacclimation in the marine diatom Skeletonema costatum, Limnol. Oceanogr. 45 (2000) 1807–1817.

68. Cruz S., Serôdio J., Relationship of rapid light curves of variable fluorescence to photoacclimation and non-photochemical quenching in a benthic diatom, Aquat. Bot. 88 (2008) 256–264. doi: 10.1016/j.aquabot.2007.11.001

69. Behrenfeld M.J., Prasil O., Babin M., Bruyant F., In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis1, J. Phycol. 40 (2004) 4–25. doi: 10.1046/j.1529-8817.2004.03083.x

70. Turpin D.H., Effects of inorganic N availability on algal photosynthesis and carbon metabolism, J. Phycol. 27 (1991) 14–20.

71. Beardall J., Young E., Roberts S., Approaches for determining phytoplankton nutrient limitation, Aquat. Sci. 63 (2001) 44–69. doi: 10.1007/PL00001344

72. Alipanah L., Rohloff J., Winge P., Bones A.M., Brembu T., Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum, J. Exp. Bot. 66 (2015) 6281–6296. doi: 10.1093/jxb/erv340 26163699

73. Mamaeva A., Namsaraev Z., Maltsev Y., Gusev E., Kulikovskiy M., Petrushkina M., Filimonova A., Sorokin B., Zotko N., Vinokurov V., Simultaneous increase in cellular content and volumetric concentration of lipids in Bracteacoccus bullatus cultivated at reduced nitrogen and phosphorus concentrations, J. Appl. Phycol. 30 (2018) 2237–2246.

74. Beardall J., Berman T., Heraud P., Kadiri M.O., Light B.R., Patterson G., Roberts S., Sulzberger B., Sahan E., Uehlinger U., A comparison of methods for detection of phosphate limitation in microalgae, Aquat. Sci. 63 (2001) 107–121.

75. Zulu N.N., Zienkiewicz K., Vollheyde K., Feussner I., Current trends to comprehend lipid metabolism in diatoms, Prog. Lipid Res. (2018).

76. Goldman J.C., Dennis J.M. Jr, Effect of large marine diatoms growing at low light on episodic new production, Limnol. Oceanogr. 48 (2003) 1176–1182.

77. Davis C.O., Continuous culture of marine diatoms under silicate limitation. Ii. Effect of light intensity on growth and nutrient uptake of Skeletonema costatum,2, J. Phycol. 12 (1976) 291–300. doi: 10.1111/j.1529-8817.1976.tb02847.x

78. Cade-Menun B.J., Paytan A., Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae, Mar. Chem. 121 (2010) 27–36. doi: 10.1016/j.marchem.2010.03.002

79. Lai J., Yu Z., Song X., Cao X., Han X., Responses of the growth and biochemical composition of Prorocentrum donghaiense to different nitrogen and phosphorus concentrations, J. Exp. Mar. Biol. Ecol. 405 (2011) 6–17. doi: 10.1016/j.jembe.2011.05.010

80. Dean A.P., Sigee D.C., Estrada B., Pittman J.K., Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae, Bioresour. Technol. 101 (2010) 4499–4507. doi: 10.1016/j.biortech.2010.01.065 20153176

81. Yi Z., Xu M., Di X., Brynjolfsson S., Fu W., Exploring valuable lipids in diatoms, Front. Mar. Sci. 4 (2017). doi: 10.3389/fmars.2017.00017

82. Olga Sayanova, Virginie Mimouni, Lionel Ulmann, Annick Morant-Manceau, Virginie Pasquet, Schoefs Benoît Napier Johnathan A., Modulation of lipid biosynthesis by stress in diatoms, Philos. Trans. R. Soc. B Biol. Sci. 372 (2017) 20160407. doi: 10.1098/rstb.2016.0407 28717017

83. Vårum K.M., Myklestad S., Effects of light, salinity and nutrient limitation on the production of β-1,3-d-glucan and exo-d-glucanase activity in Skeletonema costatum (Grev.) Cleve, J. Exp. Mar. Biol. Ecol. 83 (1984) 13–25. doi: 10.1016/0022-0981(84)90114-X

84. Huntley M.E., Johnson Z.I., Brown S.L., Sills D.L., Gerber L., Archibald I., Machesky S.C., Granados J., Beal C., Greene C.H., Demonstrated large-scale production of marine microalgae for fuels and feed, Algal Res. 10 (2015) 249–265. doi: 10.1016/j.algal.2015.04.016

85. Kates M., Volcani B.E., Lipid components of diatoms, Biochim. Biophys. Acta BBA—Lipids Lipid Metab. 116 (1966) 264–278. doi: 10.1016/0005-2760(66)90009-9

86. Chen G., Jiang Y., Chen F., Fatty acid and lipid class composition of the eicosapentaenoic acid-producing microalga, Nitzschia laevis, Food Chem. 104 (2007) 1580–1585. doi: 10.1016/j.foodchem.2007.03.008

87. Volkman J.K., Eglinton G., Corner E.D.S., Sterols and fatty acids of the marine diatom Biddulphia sinensis, Phytochemistry. 19 (1980) 1809–1813. doi: 10.1016/S0031-9422(00)83818-2

88. Jiang H., Gao K., Effects of Lowering Temperature During Culture on the Production of Polyunsaturated Fatty Acids in the Marine Diatom Phaeodactylum Tricornutum (bacillariophyceae)1, J. Phycol. 40 (2004) 651–654. doi: 10.1111/j.1529-8817.2004.03112.x

89. Ackman R.G., Jangaard P.M., Hoyle R.J., Brockerhoff H., Origin of marine fatty acids. I. Analyses of the fatty acids produced by the diatom Skeletonema costatum, J. Fish. Res. Board Can. 21 (1964) 747–756. doi: 10.1139/f64-067

90. Griffiths M.J., van Hille R.P., Harrison S.T.L., Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions, J. Appl. Phycol. 24 (2012) 989–1001. doi: 10.1007/s10811-011-9723-y

91. Plumley F.G., Schmidt G.W., Nitrogen-dependent regulation of photosynthetic gene expression, Proc. Natl. Acad. Sci. 86 (1989) 2678–2682. doi: 10.1073/pnas.86.8.2678 16594026

92. Yu E.T., Zendejas F.J., Lane P.D., Gaucher S., Simmons B.A., Lane T.W., Triacylglycerol accumulation and profiling in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Baccilariophyceae) during starvation, J. Appl. Phycol. 21 (2009) 669. doi: 10.1007/s10811-008-9400-y

93. Xia S., Wan L., Li A., Sang M., Zhang C., Effects of nutrients and light intensity on the growth and biochemical composition of a marine microalga Odontella aurita, Chin. J. Oceanol. Limnol. 31 (2013) 1163–1173. doi: 10.1007/s00343-013-2092-4

94. Griffiths M.J., Harrison S.T.L., Lipid productivity as a key characteristic for choosing algal species for biodiesel production, J. Appl. Phycol. 21 (2009) 493–507. doi: 10.1007/s10811-008-9392-7

95. Pessôa M.G., Vespermann K.A.C., Paulino B.N., Barcelos M.C.S., Pastore G.M., Molina G., Newly isolated microorganisms with potential application in biotechnology, Biotechnol. Adv. 37 (2019) 319–339. doi: 10.1016/j.biotechadv.2019.01.007 30664944

96. Amaro H.M., Guedes A.C., Malcata F.X., Advances and perspectives in using microalgae to produce biodiesel, Appl. Energy. 88 (2011) 3402–3410. doi: 10.1016/j.apenergy.2010.12.014

97. Sharma K.K., Schuhmann H., Schenk P.M., High lipid induction in microalgae for biodiesel production, Energies. 5 (2012) 1532–1553. doi: 10.3390/en5051532

98. Ozkan A., Kinney K., Katz L., Berberoglu H., Reduction of water and energy requirement of algae cultivation using an algae biofilm photobioreactor, Bioresour. Technol. 114 (2012) 542–548. doi: 10.1016/j.biortech.2012.03.055 22503193

99. Tian X., Liao Q., Zhu X., Wang Y., Zhang P., Li J., Wang H., Characteristics of a biofilm photobioreactor as applied to photo-hydrogen production, Bioresour. Technol. 101 (2010) 977–983. doi: 10.1016/j.biortech.2009.09.007 19818607

100. Schultze L.K., Simon M.-V., Li T., Langenbach D., Podola B., Melkonian M., High light and carbon dioxide optimize surface productivity in a Twin-Layer biofilm photobioreactor, Algal Res. 8 (2015) 37–44.

101. Silva-Aciares F.R., Riquelme C.E., Comparisons of the growth of six diatom species between two configurations of photobioreactors, Aquac. Eng. 38 (2008) 26–35. doi: 10.1016/j.aquaeng.2007.10.005


Článek vyšel v časopise

PLOS One


2019 Číslo 11