Physiological and transcriptome analysis elucidates the metabolic mechanism of versatile Porphyridium purpureum under nitrogen deprivation for exopolysaccharides accumulation

Liang Ji , Shaohua Li , Cheng Chen , Haojie Jin , Haizhen Wu , Jianhua Fan

Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 73

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Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 73 DOI: 10.1186/s40643-021-00426-x
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Physiological and transcriptome analysis elucidates the metabolic mechanism of versatile Porphyridium purpureum under nitrogen deprivation for exopolysaccharides accumulation

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Abstract

Porphyridium purpureum is a mesophilic, unicellular red alga rich in phycoerythrin, sulfate polysaccharides, and polyunsaturated fatty acids. Nitrogen deficiency inhibited the growth of P. purpureum and resulted in yellowing of the cells and thickening of the extracellular viscousness sheath. Under nitrogen stress, the contents of total lipids and exopolysaccharides in P. purpureum were increased by 65.2% and 188.0%, respectively. We demonstrate that the immediate response of P. purpureum to nitrogen deficiency is mediated by carbon flow to polysaccharide synthesis, while the synthesis of lipids is enhanced as a permanent energy storage substance at the later stage. Based on transcriptome annotation information, we elucidate the synthesis pathway of polysaccharides from P. purpureum from the perspective of glycosyl-donor interconversion, and demonstrate that the n-6 pathway is the main synthesis pathway of polyunsaturated fatty acids. This study not only provides a production strategy for polysaccharides and fatty acids by single-celled marine red algae P. purpureum, but also provides targets for further genetic modification.

Keywords

Porphyridium purpureum / Nitrogen deprivation / Transcriptome analysis / Exopolysaccharides / Polyunsaturated fatty acids / Phycoerythrin

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Liang Ji, Shaohua Li, Cheng Chen, Haojie Jin, Haizhen Wu, Jianhua Fan. Physiological and transcriptome analysis elucidates the metabolic mechanism of versatile Porphyridium purpureum under nitrogen deprivation for exopolysaccharides accumulation. Bioresources and Bioprocessing, 2021, 8(1): 73 DOI:10.1186/s40643-021-00426-x

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References

[1]

Adir N, Bar-Zvi S, Harris D. (2020) The amazing phycobilisome. Biochim Biophys Acta Bioenerg, 1861, 4: 148047.

[2]

Aksmann A, Tukaj Z. Intact anthracene inhibits photosynthesis in algal cells: a fluorescence induction study on Chlamydomonas reinhardtii Cw92 strain. Chemosphere, 2008, 74(1): 26-32.

[3]

Arad SM, Friedman OD, Rotem A. Effect of nitrogen on polysaccharide production in a Porphyridium sp. Appl Environ Microbiol, 1988, 54(10): 2411.

[4]

Arsiya F, Sayadi MH, Sobhani S. Green synthesis of palladium nanoparticles using Chlorellavulgaris. Mater Lett, 2017, 186: 113-115.

[5]

Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N, Ball S, Weber AP, Arias MC, Henrissat B, Coutinho PM, Krishnan A, Zauner S, Morath S, Hilliou F, Egizi A, Perrineau MM, Yoon HS. Genome of the red alga Porphyridiumpurpureum. Nat Commun, 2013, 4: 1941.

[6]

Corteggiani Carpinelli E, Telatin A, Vitulo N, Forcato C, D'Angelo M, Schiavon R, Vezzi A, Giacometti GM, Morosinotto T, Valle G. Chromosome scale genome assembly and transcriptome profiling of Nannochloropsisgaditana in nitrogen depletion. Mol Plant, 2014, 7(2): 323-335.

[7]

Ficko-Blean E, Hervé C, Michel G. Sweet and sour sugars from the sea: the biosynthesis and remodeling of sulfated cell wall polysaccharides from marine macroalgae. Perspect Phycol, 2015, 2(1): 51-64.

[8]

Gloaguen V, Ruiz G, Morvan H, Mouradi-Givernaud A, Maes E, Krausz P, Strecker G. The extracellular polysaccharide of Porphyridium sp.: an NMR study of lithium-resistant oligosaccharidic fragments. Carbohydr Res, 2004, 339(1): 97-103.

[9]

Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J, 2008, 54(4): 621-639.

[10]

Jaeger D, Winkler A, Mussgnug JH, Kalinowski J, Goesmann A, Kruse O. Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidiumneglectum reveal a model for triacylglycerol and lipid hyperaccumulation. Biotechnol Biofuels, 2017, 10: 197.

[11]

Jeon MS, Han SI, Jeon M, Choi YE. Enhancement of phycoerythrin productivity in Porphyridiumpurpureum using the clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 ribonucleoprotein system. Bioresour Technol, 2021, 330: 124974.

[12]

Jia SY. Effects of different concentration of salinity, nitrogen and phosphorus on growth and metabolism of Porphyridiumpurpureum, 2006, Dalian: Dalian University of Technology.

[13]

Jiao KL, Xiao WP, Shi XG, Ho SH, Chang JS, Ng IS, Tang X, Sun Y, Zeng XH, Lin L. Molecular mechanism of arachidonic acid biosynthesis in Porphyridiumpurpureum promoted by nitrogen limitation. Bioprocess Biosyst Eng, 2021

[14]

Kannaujiya VK, Sinha RP. Thermokinetic stability of phycocyanin and phycoerythrin in food-grade preservatives. J Appl Phycol, 2015, 28(2): 1063-1070.

[15]

Khozin I, Adlerstein D, Bigongo C, Heimer YM, Cohen Z. Elucidation of the biosynthesis of eicosapentaenoic acid in the microalga Porphyridiumcruentum (II. Studies with radiolabeled precursors). Plant Physiol, 1997, 114: 223-230.

[16]

Khozin-Goldberg I, Iskandarov U, Cohen Z. LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl Microbiol Biotechnol, 2011, 91(4): 905-915.

[17]

Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods, 2015, 12(4): 357-360.

[18]

Kurpan Nogueira DP, Silva AF, Araújo OQF, Chaloub RM. Impact of temperature and light intensity on triacylglycerol accumulation in marine microalgae. Biomass Bioenergy, 2015, 72: 280-287.

[19]

Levitan O, Dinamarca J, Zelzion E, Lun DS, Guerra LT, Kim MK, Kim J, Van Mooy BA, Bhattacharya D, Falkowski PG. Remodeling of intermediate metabolism in the diatom Phaeodactylumtricornutum under nitrogen stress. Proc Natl Acad Sci USA, 2015, 112(2): 412-417.

[20]

Li ZC, Bock R. Replication of bacterial plasmids in the nucleus of the red alga Porphyridiumpurpureum. Nat Commun, 2018, 9(1): 3451.

[21]

Li J, Han DX, Wang DM, Ning K, Jia J, Wei L, Jing XY, Huang S, Chen J, Li YT, Hu Q, Xu J. Choreography of transcriptomes and lipidomes of nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell, 2014, 26(4): 1645-1665.

[22]

Li XT, Li W, Zhai J, Wei HX. Effect of nitrogen limitation on biochemical composition and photosynthetic performance for fed-batch mixotrophic cultivation of microalga Spirulinaplatensis. Bioresour Technol, 2018, 263: 555-561.

[23]

Li SH, Ji L, Shi QW, Wu HZ, Fan JH. Advances in the production of bioactive substances from marine unicellular microalgae Porphyridium spp. Bioresour Technol, 2019, 292: 122048.

[24]

Li SH, Ji L, Chen C, Zhao SX, Sun M, Gao ZQ, Wu HZ, Fan JH. Efficient accumulation of high-value bioactive substances by carbon to nitrogen ratio regulation in marine microalgae Porphyridiumpurpureum. Bioresour Technol, 2020, 309: 123362.

[25]

Liang CW, Cao SN, Zhang XW, Zhu BH, Su ZL, Xu D, Guang XY, Ye NN. De novo sequencing and global transcriptome analysis of Nannochloropsis sp. (Eustigmatophyceae) following nitrogen starvation. Bioenerg Res, 2012, 6(2): 494-505.

[26]

Liang JB, Wen F, Liu JH. Transcriptomic and lipidomic analysis of an EPA-containing Nannochloropsis sp. PJ12 in response to nitrogen deprivation. Sci Rep, 2019, 9(1): 4540.

[27]

Liu J, Sun Z, Mao XM, Gerken H, Wang XF, Yang WQ. Multiomics analysis reveals a distinct mechanism of oleaginousness in the emerging model alga Chromochloriszofingiensis. Plant J, 2019, 98(6): 1060-1077.

[28]

Ma JF, You X, Sun S, Wang XX, Qin S, Sui SF. Structural basis of energy transfer in Porphyridiumpurpureum phycobilisome. Nature, 2020, 579(7797): 146-151.

[29]

Mao XZ, Cai T, Olyarchuk JG, Wei LP. Automated genome annotation and pathway identification using the KEGG orthology (KO) as a controlled vocabulary. Bioinformatics, 2005, 21(19): 3787-3793.

[30]

Miller R, Wu GX, Deshpande RR, Vieler A, Gartner K, Li XB, Moellering ER, Zauner S, Cornish AJ, Liu BS, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C. Changes in transcript abundance in Chlamydomonasreinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol, 2010, 154(4): 1737-1752.

[31]

Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H. Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonasreinhardtii and Coccomyxa sp. C-169. Phytochemistry, 2012, 75: 50-59.

[32]

Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol, 2015, 33(3): 290-295.

[33]

Prasad B, Lein W, Thiyam G, Lindenberger CP, Buchholz R, Vadakedath N. Stable nuclear transformation of rhodophyte species Porphyridiumpurpureum: advanced molecular tools and an optimized method. Photosynth Res, 2019, 140(2): 173-188.

[34]

Renaud SM, Thinh LV, Lambrinidis G, Parry DL. Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture, 2002, 211(1–4): 195-214.

[35]

Schmollinger S, Muhlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, Hemme D, Pellegrini M, Grossman AR, Stitt M, Schroda M, Merchant SS. Nitrogen-sparing mechanisms in chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell, 2014, 26(4): 1410-1435.

[36]

Shiran D, Khozin I, Heimer YM, Cohen Z. Biosynthesis of eicosapentaenoic acid in the microalga Porphyridiumcruentum. I: The use of externally supplied fatty acids. Lipids, 1996, 31(12): 1277-1282.

[37]

Siaut M. Oil accumulation in the model green alga Chlamydomonasreinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol, 2011, 11: 1-15.

[38]

Skriptsova AV. Fucoidans of brown algae: biosynthesis, localization, and physiological role in thallus. Russ J Mar Biol, 2015, 41(3): 145-156.

[39]

Sun LQ, Wang CH, Shi QJ, Ma CH. Preparation of different molecular weight polysaccharides from Porphyridiumcruentum and their antioxidant activities. Int J Biol Macromol, 2009, 45(1): 42-47.

[40]

Sun DY, Zhu JQ, Fang L, Zhang X, Chow Y, Liu JH. De novo transcriptome profiling uncovers a drastic downregulation of photosynthesis upon nitrogen deprivation in the nonmodel green alga Botryosphaerellasudeticus. BMC Genomics, 2013, 14: 1-18.

[41]

Timilsena YP, Wang B, Adhikari R, Adhikari B. Advances in microencapsulation of polyunsaturated fatty acids (PUFAs)-rich plant oils using complex coacervation: a review. Food Hydrocoll, 2017, 69: 369-381.

[42]

Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 2010, 26(1): 136-138.

[43]

Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol, 2010, 11(2): 1-12.

[44]

Zhao Y, Hou YY, Chai WJ, Liu ZY, Wang X, He CQ, Hu ZP, Chen SL, Wang WJ, Chen FJ. Transcriptome analysis of Haematococcuspluvialis of multiple defensive systems against nitrogen starvation. Enzyme Microb Technol, 2020, 134: 109487.

Funding

National Key Research and Development Project of China(2019YFA0906300)

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