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Cited by 238Algal biology and biofuel productionMicrobial Metabolic Engineering and BioproductionAquaculture Nutrition and Growth

Nitrogen starvation-induced cellular crosstalk of ROS-scavenging antioxidants and phytohormone enhanced the biofuel potential of green microalga Acutodesmus dimorphus

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Chokshi, Kaumeel, Pancha, Imran, Ghosh, Arup, Mishra, Sandhya·2017·Biotechnology for Biofuels
DOI 10.1186/s13068-017-0747-7PMC PMC5345260
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Abstract

Microalgae accumulate a considerable amount of lipids and carbohydrate under nutrient-deficient conditions, which makes them one of the promising sustainable resources for biofuel production. In the present study, to obtain the biomass with higher lipid and carbohydrate contents, we implemented a short-term nitrogen starvation of 1, 2, and 3 days in a green microalga Acutodesmus dimorphus . Few recent reports suggest that oxidative stress-tolerant microalgae are highly efficient for biofuel production. To study the role of oxidative stress due to nitrogen deficiency, responses of various stress biomarkers like reactive oxygen species (ROS), cellular enzymatic antioxidants superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and non-enzymatic scavengers proline and polyphenols were also evaluated. Further, the endogenous levels of phytohormones abscisic acid (ABA) and indole-3-acetic acid (IAA) were also determined to study their response to nitrogen deficiency. We observed that nitrogen starvation of 2 days is effective to produce biomass containing 29.92% of lipid (comprising about 75% of neutral lipid) and 34.80% of carbohydrate, which is significantly higher (about 23 and 64%, respectively) than that of the control culture. Among all nitrogen-starved cultures, the accumulations of ROS were lower in 2 days starved culture, which can be linked with the several folds higher activities of SOD and CAT in this culture. The accumulations of proline and total polyphenols were also significantly higher (about 4.7- and 1.7-folds, respectively, than that of the control) in 2 days nitrogen-starved culture. The levels of phytohormones once decreased significantly after 1 day, increased continuously up to 3 days of nitrogen starvation. The findings of the present study highlight the interaction of nitrogen starvation-induced oxidative stress with the signaling involved in the growth and development of microalga. The study presents a comprehensive picture of the adaptive mechanisms of the cells from a physiological perspective along with providing the strategy to improve the biofuel potential of A. dimorphus through a short-term nitrogen starvation.

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  • Nitrogen deficiency serves as a significant stimulus for lipid accumulation in various microalgae species, such as Acutodesmus dimorphus, Nephrochlamys yushanlensis, C. vulgaris, Scenedesmus quadricauda, and N. oceanica.

    “Nitrogen deficiency serves as a significant stimulus for lipid accumulation in various microalgae species, such as Acutodesmus dimorphus [106], Nephrochlamys yushanlensis [107, 108], C. vulgaris [109], Scenedesmus quadricauda [110], and N. oceanica [111].”

    From Microalgae biofuels: illuminating the path to a sustainable future amidst challenges and opportunities (2024) · cites this paper as [106]

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References 72 · Cited by 238

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  1. [3]George B Pancha I Desai C Chokshi K Paliwal C Ghosh T Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus—a potential strain for bio-fuel production Bioresour Technol 2014 171 367 374 10.1016/j.biortech.2014.08.086 25218209 · DOI · Paper page
  2. [4]Chokshi K Pancha I Trivedi K George B Maurya R Ghosh A Biofuel potential of the newly isolated microalgae Acutodesmus dimorphus under temperature induced oxidative stress conditions Bioresour Technol 2015 180 162 171 10.1016/j.biortech.2014.12.102 25600013 · DOI
  3. [6]Peccia J Haznedaroglu B Gutierrez J Zimmerman JB Nitrogen supply is an important driver of sustainable microalgae biofuel production Trends Biotechnol 2013 31 134 138 10.1016/j.tibtech.2013.01.010 23414785 · DOI
  4. [7]Chen M Tang H Ma H Holland TC Ng KYS Salley SO Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta Bioresour Technol 2011 102 1649 1655 10.1016/j.biortech.2010.09.062 20947341 · DOI
  5. [8]Mallick N Mohn FH Reactive oxygen species: response of algal cells J Plant Physiol 2000 157 183 193 10.1016/S0176-1617(00)80189-3 · DOI
  6. [9]Cirulis JT Scott JA Ross GM Management of oxidative stress by microalgae Can J Physiol Pharmacol 2013 91 15 21 10.1139/cjpp-2012-0249 23368282 · DOI
  7. [10]Xin L Hong-ying H Yu-ping Z Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature Bioresour Technol 2011 102 3098 3102 10.1016/j.biortech.2010.10.055 21055924 · DOI
  8. [11]Pancha I Chokshi K Maurya R Trivedi K Patidar SK Ghosh A Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077 Bioresour Technol 2015 189 341 348 10.1016/j.biortech.2015.04.017 25911594 · DOI
  9. [12]Yilancioglu K Cokol M Pastirmaci I Erman B Cetiner S Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain PLoS ONE 2014 9 e91957 10.1371/journal.pone.0091957 24651514 PMC3961284 · DOI
  10. [13]Zhang YM Chen H He CL Wang Q Nitrogen starvation induced oxidative stress in an oil-producing green alga Chlorella sorokiniana C3 PLoS ONE 2013 8 e69225 10.1371/journal.pone.0069225 23874918 PMC3712941 · DOI
  11. [14]Menon KR Balan R Suraishkumar GK Stress induced lipid production in Chlorella vulgaris: relationship with specific intracellular reactive species levels Biotechnol Bioeng 2013 110 1627 1636 10.1002/bit.24835 23297178 · DOI
  12. [15]Petrov VD Van Breusegem F Hydrogen peroxide-a central hub for information flow in plant cells AoB Plants 2012 2012 pls014 10.1093/aobpla/pls014 22708052 PMC3366437 · DOI
  13. [16]Wrzaczek M Brosché M Kangasjärvi J ROS signaling loops—production, perception, regulation Curr Opin Plant Biol 2013 16 575 582 10.1016/j.pbi.2013.07.002 23876676 · DOI
  14. [17]Lu Y Xu J Phytohormones in microalgae: a new opportunity for microalgal biotechnology? Trends Plant Sci 2015 20 273 282 10.1016/j.tplants.2015.01.006 25697753 · DOI
  15. [18]Chokshi K Pancha I Maurya R Paliwal C Ghosh T Ghosh A Growth medium standardization and thermotolerance study of the freshwater microalga Acutodesmus dimorphus—a potential strain for biofuel production J Appl Phycol 2016 28 2687 2696 10.1007/s10811-016-0826-3 · DOI
  16. [19]Chokshi K Pancha I Ghosh A Mishra S Microalgal biomass generation by phycoremediation of dairy industry wastewater: an integrated approach towards sustainable biofuel production Bioresour Technol 2016 221 455 460 10.1016/j.biortech.2016.09.070 27668878 · DOI
  17. [20]Lichtenthaler HK Chlorophylls and carotenoids: pigments of photosynthetic biomembranes Methods Enzymol 1987 148 350 382 10.1016/0076-6879(87)48036-1 · DOI · Paper page
  18. [25]Becker EW Microalgae: biotechnology and microbiology 1994 Cambridge Cambridge University Press
  19. [26]Hodges DM DeLong JM Forney CF Prange RK Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds Planta 1999 207 604 611 10.1007/s004250050524 28456836 · DOI
  20. [28]Liu Y Jiang H Zhao Z An L Nitric oxide synthase like activity-dependent nitric oxide production protects against chilling-induced oxidative damage in Chorispora bungeana suspension cultured cells Plant Physiol Biochem 2010 48 936 944 10.1016/j.plaphy.2010.09.001 20875746 · DOI
  21. [29]Halliwell B Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life Plant Physiol 2006 141 312 322 10.1104/pp.106.077073 16760481 PMC1475431 · DOI
  22. [30]Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051 · DOI · Paper page
  23. [33]Chandler SF Dodds JH The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum Plant Cell Rep 1983 2 205 208 10.1007/BF00270105 24258053 · DOI
  24. [34]Pan X Welti R Wang X Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry Nat Protoc 2010 5 986 992 10.1038/nprot.2010.37 20448544 · DOI
  25. [35]Sulochana SB Arumugam M Influence of abscisic acid on growth, biomass and lipid yield of Scenedesmus quadricauda under nitrogen-starved condition Bioresour Technol 2016 213 198 203 10.1016/j.biortech.2016.02.078 26949054 · DOI
  26. [37]Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans Appl Microbiol Biotechnol 2008 81 629 636 10.1007/s00253-008-1681-1 18795284 · DOI · Paper page
  27. [38]Markou G Depraetere O Muylaert K Effect of ammonia on the photosynthetic activity of Arthrospira and Chlorella: a study on chlorophyll fluorescence and electron transport Algal Res 2016 16 449 457 10.1016/j.algal.2016.03.039 · DOI
  28. [39]Goiris K Van Colen W Wilches I León-Tamariz F De Cooman L Muylaert K Impact of nutrient stress on antioxidant production in three species of microalgae Algal Res 2015 7 51 57 10.1016/j.algal.2014.12.002 · DOI
  29. [40]Kalaji HM Schansker G Ladle RJ Goltsev V Bosa K Allakhverdiev SI Frequently asked questions about in vivo chlorophyll fluorescence: practical issues Photosynth Res 2014 122 121 158 10.1007/s11120-014-0024-6 25119687 PMC4210649 · DOI
  30. [41]Ördög V Stirk WA Bálint P van Staden J Lovász C Changes in lipid, protein and pigment concentrations in nitrogen-stressed Chlorella minutissima cultures J Appl Phycol 2012 24 907 914 10.1007/s10811-011-9711-2 · DOI
  31. [42]Li J Han D Wang D Ning K Jia J Wei L Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae Plant Cell 2014 26 1645 1665 10.1105/tpc.113.121418 24692423 PMC4036577 · DOI · Paper page
  32. [43]Turpin DH Effects of inorganic n availability on algal photosynthesis and carbon metabolism J Phycol 1991 27 14 20 10.1111/j.0022-3646.1991.00014.x · DOI
  33. [44]Adams C Godfrey V Wahlen B Seefeldt L Bugbee B Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae Bioresour Technol 2013 131 188 194 10.1016/j.biortech.2012.12.143 23347926 · DOI · Paper page
  34. [45]Courchesne NMD Parisien A Wang B Lan CQ Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches J Biotechnol 2009 141 31 41 10.1016/j.jbiotec.2009.02.018 19428728 · DOI
  35. [46]Mujtaba G Choi W Lee C-G Lee K Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions Bioresour Technol 2012 123 279 283 10.1016/j.biortech.2012.07.057 22940330 · DOI
  36. [47]Jia J Han D Gerken HG Li Y Sommerfeld M Hu Q Molecular mechanisms for photosynthetic carbon partitioning into storage neutral lipids in Nannochloropsis oceanica under nitrogen-depletion conditions Algal Res 2015 7 66 77 10.1016/j.algal.2014.11.005 · DOI
  37. [48]Fan J Andre C Xu C A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii FEBS Lett 2011 585 1985 1991 10.1016/j.febslet.2011.05.018 21575636 · DOI · Paper page
  38. [49]Zhu S Huang W Xu J Wang Z Xu J Yuan Z Metabolic changes of starch and lipid triggered by nitrogen starvation in the microalga Chlorella zofingiensis Bioresour Technol 2014 152 292 298 10.1016/j.biortech.2013.10.092 24308944 · DOI
  39. [50]Pancha I Chokshi K Maurya R Bhattacharya S Bachani P Mishra S Comparative evaluation of chemical and enzymatic saccharification of mixotrophically grown de-oiled microalgal biomass for reducing sugar production Bioresour Technol 2016 204 9 16 10.1016/j.biortech.2015.12.078 26771924 · DOI
  40. [51]Fan J Yan C Andre C Shanklin J Schwender J Xu C Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii Plant Cell Physiol 2012 53 1380 1390 10.1093/pcp/pcs082 22642988 · DOI
  41. [52]Gill SS Tuteja N Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants Plant Physiol Biochem 2010 48 909 930 10.1016/j.plaphy.2010.08.016 20870416 · DOI
  42. [53]Ruiz-Domínguez MC Vaquero I Obregón V de la Morena B Vílchez C Vega JM Lipid accumulation and antioxidant activity in the eukaryotic acidophilic microalga Coccomyxa sp. (strain onubensis) under nutrient starvation J Appl Phycol 2015 27 1099 1108 10.1007/s10811-014-0403-6 · DOI
  43. [54]Salbitani G Vona V Bottone C Petriccione M Carfagna S Sulfur deprivation results in oxidative perturbation in Chlorella sorokiniana (211/8k) Plant Cell Physiol 2015 56 897 905 10.1093/pcp/pcv015 25647328 · DOI
  44. [55]Yoshida K Igarashi E Mukai M Hirata K Miyamoto K Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid Plant Cell Environ 2003 26 451 457 10.1046/j.1365-3040.2003.00976.x · DOI
  45. [56]Ashraf M Foolad MR Roles of glycine betaine and proline in improving plant abiotic stress resistance Environ Exp Bot 2007 59 206 216 10.1016/j.envexpbot.2005.12.006 · DOI
  46. [57]Trovato M Mattioli R Costantino P Multiple roles of proline in plant stress tolerance and development Rend Lincei 2008 19 325 346 10.1007/s12210-008-0022-8 · DOI
  47. [58]Parida AK Jha B Inductive responses of some organic metabolites for osmotic homeostasis in peanut (Arachis hypogaea L.) seedlings during salt stress Acta Physiol Plant 2013 35 2821 2832 10.1007/s11738-013-1315-9 · DOI
  48. [59]Kováčik J Klejdus B Bačkor M Physiological responses of Scenedesmus quadricauda (Chlorophyceae) to UV-A and UV-C light Photochem Photobiol 2010 86 612 616 10.1111/j.1751-1097.2010.00708.x 20202162 · DOI
  49. [60]Duval B Shetty K Thomas WH Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light J Appl Phycol 1999 11 559 566 10.1023/A:1008178208949 · DOI
  50. [61]Noctor G Lelarge-Trouverie C Mhamdi A The metabolomics of oxidative stress Phytochemistry 2015 112 33 53 10.1016/j.phytochem.2014.09.002 25306398 · DOI
  51. [62]Wu S Meng Y Cao X Xue S Regulatory mechanisms of oxidative species and phytohormones in marine microalgae Isochrysis zhangjiangensis under nitrogen deficiency Algal Res 2016 17 321 329 10.1016/j.algal.2016.05.025 · DOI
  52. [65]Salama ES Kabra AN Ji MK Kim JR Min B Jeon BH Enhancement of microalgae growth and fatty acid content under the influence of phytohormones Bioresour Technol 2014 172 97 103 10.1016/j.biortech.2014.09.002 25247249 · DOI
  53. [66]El Arroussi H Benhima R Bennis I El Mernissi N Wahby I Improvement of the potential of Dunaliella tertiolecta as a source of biodiesel by auxin treatment coupled to salt stress Renew Energy 2015 77 15 19 10.1016/j.renene.2014.12.010 · DOI
  54. [67]Liu J Qiu W Song Y Stimulatory effect of auxins on the growth and lipid productivity of Chlorella pyrenoidosa and Scenedesmus quadricauda Algal Res 2016 18 273 280 10.1016/j.algal.2016.06.027 · DOI
  55. [68]Lu Y Tarkowska D Turečková V Luo T Xin Y Li J Antagonistic roles of abscisic acid and cytokinin during response to nitrogen depletion in oleaginous microalga Nannochloropsis oceanica expand the evolutionary breadth of phytohormone function Plant J 2014 80 52 68 10.1111/tpj.12615 25041627 · DOI
  56. [69]Saradhi PP Suzuki I Katoh A Sakamoto A Sharmila P Shi D-J Protection against the photo-induced inactivation of the photosystem II complex by abscisic acid Plant Cell Environ 2000 23 711 718 10.1046/j.1365-3040.2000.00579.x · DOI

Authors
Chokshi, K., Pancha, I., Ghosh, A., & Mishra, S.
Affiliations
  • Central Salt and Marine Chemicals Research Institute (IN)
  • Tokyo Institute of Technology (JP)
Corresponding author
  • Ghosh, Arup
  • Mishra, Sandhya
ORCID
Venue
Biotechnology for Biofuels
Publisher
Springer Science and Business Media LLC
Published
2017-03-09
Volume
10
Issue
1
Pages
60-60
ISSN
1754-6834 (ISSN-L)
DOI
10.1186/s13068-017-0747-7
PMC
PMC5345260
OpenAlex
W2594873865
Cited by
238
References
72
Citations by year
2026: 16 · 2025: 30 · 2024: 31 · 2023: 24 · 2022: 27 · 2021: 26 · 2020: 36 · 2019: 22 · 2018: 18 · 2017: 8
FWCI
6.15
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Biotechnology for Biofuels (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Council of Scientific and Industrial Research (CSC-0203)
Topics
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
Keywords
nitrogen starvation, oxidative stress, reactive oxygen species, antioxidant enzymes, superoxide dismutase, catalase, ascorbate peroxidase, proline, polyphenols, abscisic acid, indole-3-acetic acid, plant hormones, lipid accumulation, carbohydrate accumulation, microalgal biofuels, stress tolerance

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