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Photosynthetic pigment production and metabolic and lipidomic alterations in the marine cyanobacteria Synechocystis sp. PCC 7338 under various salinity conditions

Abstract

Synechocystis sp. PCC 7338 (hereafter referred to as Synechocystis 7338) is a marine cyanobacterium that has the potential to produce photosynthetic pigments. In this study, we investigated the effects of various NaCl concentrations (0, 0.4, 0.8, and 1.2 M) on cell growth, photosynthetic pigments, and metabolites and intact lipid species profiles in Synechocystis 7338. The overall growth pattern of Synechocystis 7338 was similar under 0, 0.4, and 0.8 M NaCl conditions. Cell growth was retarded after reaching the exponential phase under 1.2 M NaCl; however, a similar growth pattern was observed after the exponential phase under 0.4 M NaCl (control group). The highest production of chlorophyll a (4.18 mg L−1), allophycocyanin (4.08 mg L−1), and phycoerythrin (1.70 mg L−1) were achieved under 1.2 M NaCl conditions. Altered metabolic and lipidomic profiles were observed at different NaCl conditions; significantly increased relative yields of glucosylglycerol, one diacylglyceryltrimethylhomoserine, one monogalactosyldiacylglycerol, and four phosphatidylglycerol species were observed under 1.2 M NaCl conditions using gas chromatography–mass spectrometry and direct infusion–mass spectrometry analyses. In addition, it was revealed that the photosynthetic activity recovered under 1.2 M NaCl conditions in long-term culture. Hydrogen peroxide content significantly increased under 1.2 M NaCl conditions. It is believed that glutathione content also significantly increased under high salinity conditions to retain the normal functioning of Synechocystis 7338. These results indicate that high salinity conditions for Synechocystis 7338 culture could be used for the large-scale production of chlorophyll a, allophycocyanin, phycoerythrin, and other bioactive metabolites.

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References

  • Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98:529–539

    CAS  PubMed  Article  Google Scholar 

  • Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bräucker R, Cogoli A, Hemmersbach R (2002) Graviperception and graviresponse at the cellular level. In: Horneck G, Baumstak-Khan C (eds) Astrobiology. Springer, Berlin, pp 287–296

    Chapter  Google Scholar 

  • Cid A, Herrero C, Torres E, Abalde J (1995) Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters. Aquat Toxicol 31:165–174

    CAS  Article  Google Scholar 

  • De Marsac NT, Houmard J (1988) Complementary chromatic adaptation: physiological conditions and action spectra. In: Packer L, Glazer AN (eds) Methods in enzymology. Academic Press, Cambridge, pp 318–328

  • Dittmann E, Fewer DP, Neilan BA (2013) Cyanobacterial toxins: biosynthetic routes and evolutionary roots. FEMS Microbiol Rev 37:23–43

    CAS  PubMed  Article  Google Scholar 

  • Eriksson L, Johansson E, Kettaneh-Wold N et al (2006) PLS. In: Eriksson L (ed) Multi-and megavariate data analysis. Umetrics AB, Umeå, pp 63–101

    Google Scholar 

  • Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Geada P, Gkelis S, Teixeira J, Vasconcelos V, Vicente AA, Fernandes B (2017) Cyanobacterial toxins as a high value-added product. In: Gonzalez-Fernandez C, Munoz R (eds) Microalgae-based biofuels and bioproducts: from feedstock cultivation to end-products. Woodhead Publishing, Sawston, pp 401–428

    Chapter  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    CAS  PubMed  Article  Google Scholar 

  • Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123

    CAS  PubMed  Article  Google Scholar 

  • Haque F, Banayan S, Yee J, Chiang YW (2017) Extraction and applications of cyanotoxins and other cyanobacterial secondary metabolites. Chemosphere 183:164–175

    CAS  PubMed  Article  Google Scholar 

  • Herrmann AJ, Gehringer MM (2019) An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean. Geobiology 17:343–359

    CAS  PubMed  Article  Google Scholar 

  • Hong SJ, Lee CG (2008) Statistical optimization of culture media for production of phycobiliprotein by Synechocystis sp. PCC 6701. Biotechnol Bioprocess Eng 13:491–498

    CAS  Article  Google Scholar 

  • Hufiejt ME, Tremolieres A, Pineau B, Lang JK, Hatheway J, Packer L (1990) Changes in membrane lipid composition during saline growth of the fresh water cyanobacterium Synechococcus 6311. Plant Physiol 94:1512–1521

    Article  Google Scholar 

  • Ilieva V, Kondeva-Burdina M, Georgieva T, Pavlova V (2019) Toxicity of cyanobacteria. Organotropy of cyanotoxins and toxicodynamics of cyanotoxins by species. Pharmacia 66:91–97

    Article  Google Scholar 

  • Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738–744

    CAS  Article  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    CAS  PubMed  Article  Google Scholar 

  • Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290:339–348

    CAS  PubMed  Article  Google Scholar 

  • Kim ZH, Park H, Ryu YJ, Shin DW, Hong SJ, Tran HL, Lim SM, Lee GC (2015) Algal biomass and biodiesel production by utilizing the nutrients dissolved in seawater using semi-permeable membrane photobioreactors. J Appl Phycol 27:1763–1773

    CAS  Article  Google Scholar 

  • Kim SH, Lim SR, Hong SJ, Cho BK, Lee H, Lee CG, Choi HK (2016) Effect of ethephon as an ethylene-releasing compound on the metabolic profile of Chlorella vulgaris. J Agric Food Chem 64:4807–4816

    CAS  PubMed  Article  Google Scholar 

  • Kim HY, Lee H, Kim S, Jin H, Bae J, Choi H-K (2017a) Discovery of potential biomarkers in human melanoma cells with different metastatic potential by metabolic and lipidomic profiling. Sci Rep 7:1–14

    Article  CAS  Google Scholar 

  • Kim JY, Kim HY, Jeon JY, Kim DM, Zhou Y, Lee JS, Lee H, Choi H-K (2017b) Effects of coronatine elicitation on growth and metabolic profiles of Lemna paucicostata culture. PLoS One 12:e0187622

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kumar J, Singh D, Tyagi MB, Kumar A (2019) Cyanobacteria: applications in biotechnology. In: Mishra AK, Tiwari DN, Rai AN (eds) Cyanobacteria from basic science to applications. Academic Press, Amsterdam, pp 327–346

    Google Scholar 

  • Lagarde D, Beuf L, Vermaas W (2000) Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 66:64–72

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278

    CAS  PubMed  Article  Google Scholar 

  • Lee HS, Kim ZH, Park H, Lee CG (2016) Specific light uptake rates can enhance astaxanthin productivity in Haematococcus lacustris. Bioprocess Biosyst Eng 39:815–823

    CAS  PubMed  Article  Google Scholar 

  • Ludwig M, Bryant DA (2012) Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:1–14

    Google Scholar 

  • Manchanda H, Sharma V (2018) Effect of salinity and lipid content of cyanobacterium Calothrix marchica. J Biol Chem Res 35:1009–1014

  • Martins R, Fernandez N, Beiras R, Vasconcelos V (2007) Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon 50:791–799

    CAS  PubMed  Article  Google Scholar 

  • Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A, Schwidke D (2008) Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J Lipid Res 49:1137–1146

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta Bioenerg 1817:194–208

    CAS  Article  Google Scholar 

  • Mostafa EM, Tammam AA (2012) The oxidative stress caused by NaCl in Azolla caroliniana is mitigated by nitrate. J Plant Interact 7:356–366

    CAS  Article  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    CAS  Article  PubMed  Google Scholar 

  • Osanai T, Kuwahara A, Iijima H, Toyooka K, Sato M, Tanaka K, Ikeuchi M, Saito K, Hirai MY (2013) Pleiotropic effect of sigE over-expression on cell morphology, photosynthesis and hydrogen production in Synechocystis sp. PCC 6803. Plant J 76:456–465

    CAS  PubMed  Article  Google Scholar 

  • Pade N, Hagemann M (2015) Salt acclimation of cyanobacteria and their application in biotechnology. Life 5:25–49

    CAS  Article  Google Scholar 

  • Pagels F, Guedes AC, Amaro HM, Kijjoa A, Vasconcelos V (2019) Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol Adv 37:422–443

    CAS  PubMed  Article  Google Scholar 

  • Paliwal C, Mitra M, Bhayani K, Bhadadwaj SVV, Ghosh T, Dubey S, Mishra S (2017) Abiotic stresses as tools for metabolites in microalgae. Bioresour Technol 244:1216–1226

    CAS  PubMed  Article  Google Scholar 

  • Park BI, Hong SJ, Kwan CB et al (2018) Characterization of culture conditions to increase phycobiliprotein production of Synechocystis sp. PCC 7338. Abstract of the 2018 KSBB International Academica-Industry Joint Meeting 460

  • Pasteur Institution (2002) CRBIP-catalogue. http://catalogue-crbip.pasteur.fr/. Accessed 20 Sept 2019

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium(IV). Anal Biochem 139:487–492

    CAS  PubMed  Article  Google Scholar 

  • Rai AK, Abraham G (1993) Salinity tolerance and growth analysis of the cyanobacterium Anabaena doliolum. Bull Environ Contam Toxicol 51:724–731

    CAS  PubMed  Google Scholar 

  • Řezanka T, Víden I, Go JV, Dor I, Dembitsky VM (2003) Polar lipids and fatty acids of three wild cyanobacterial strains of the genus Chroococcidiopsis. Folia Microbiol (Praha) 48:781–786

    Article  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Ritter D, Yopp JH (1993) Plasma membrane lipid composition of the halophilic cyanobacterium Aphanothece halophytica. Arch Microbiol 159:435–439

    CAS  Article  Google Scholar 

  • Ruangsomboon S (2014) Effect of media and salinity on lipid content of cyanobacterium Hapalosiphon sp. Chiang Mai J Sci 41:307–315

    Google Scholar 

  • Sato N, Hagio M, Wada H, Tsuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci U S A 97:10655–10660

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Schubert H, Fulda S, Hagemann M (1993) Effects of adaptation to different salt concentrations on photosynthesis and pigmentation of the cyanobacterium Synechocystis sp. PCC 6803. J Plant Physiol 142:291–295

    CAS  Article  Google Scholar 

  • Schwarz D, Orf I, Kopka J, Hagemann M (2013) Recent applications of metabolomics toward cyanobacteria. Metabolites 3:72–100

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sharma G, Kumar M, Ali MI, Jasuja ND (2014) Effect of carbon content, salinity and pH on Spirulina platensis for phycocyanin, allophycocyanin and phycoerythrin accumulation. J Microb Biochem Technol 6:202–206

    Google Scholar 

  • Singh SC, Sinha RP, Häder DP (2002) Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool 41:297–308

    CAS  Google Scholar 

  • Stadnichuk IN, Tropin IV (2017) Phycobiliproteins: structure, functions and biotechnological applications. Appl Biochem Microbiol 53:1–10

    CAS  Article  Google Scholar 

  • Tian X, Chen L, Wang J, Qiao J, Zhang W (2013) Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. J Proteome 78:326–345

    CAS  Article  Google Scholar 

  • Tran DT, Yeh KL, Chen CL, Chang JS (2012) Enzymatic transesterification of microalgal oil from Chlorella vulgaris ESP-31 for biodiesel synthesis using immobilized Burkholderia lipase. Bioresour Technol 108:119–127

    CAS  PubMed  Article  Google Scholar 

  • Vijayakumar S, Menakha M (2015) Pharmaceutical applications of cyanobacteria-a review. J Acute Med 5:15–23

    Article  Google Scholar 

  • Wada H, Murata N (1998) Membrane lipids in cyanobacteria. In: Siegenthaler PA, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Springer, Dordrecht, pp 65–81

    Google Scholar 

  • Waditee R, Hibino T, Nakamura T, Icharoensadki A, Takabe T (2002) Overexpression of a Na+/H+ antiporter confers salt tolerance on a freshwater cyanobacterium, making it capable of growth in sea water. Proc Natl Acad Sci U S A 99:4109–4114

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Xue Y, He Q (2015) Cyanobacteria as cell factories to produce plant secondary metabolites. Front Bioeng Biotechnol 3:1–6

    Article  Google Scholar 

  • Yoshihara S, Geng X, Ikeuchi M (2002) pilG gene cluster and split pilL genes involved in pilus biogenesis, motility and genetic transformation in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 43:513–521

    CAS  PubMed  Article  Google Scholar 

  • Zahra Z, Kim S-Y, Kim H-Y, Lee H, Lee H, Jeon J-Y, Kim D-M, Kim D-M, Hong S-J, Cho B-K, Lee H, Lee C-G, Arshad M, Choi H-K (2018) Phycobiliproteins production enhancement and lipidomic alteration by titanium dioxide nanoparticles in Synechocystis sp. PCC 6803 culture. J Agric Food Chem 66:8522–8529

    CAS  PubMed  Article  Google Scholar 

  • Zakhozhii IG, Matalin DA, Popova LG, Balnokin YV (2012) Responses of photosynthetic apparatus of the halotolerant microalga Dunalliella maritima to hyperosmotic salt shock. Russ J Plant Physiol 59:42–49

    CAS  Article  Google Scholar 

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Funding

This work was supported by grants from the National Research Foundation of Korea (NRF) (NRF-2015R1A5A1008958 and NRF-2016M1A5A1027464), funded by the Korean government (MSIP).

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HL contributed to performing experiments, analysis, and interpretation of the data, and writing and revising the manuscript. YN and SH contributed to performing experiments and revising the manuscript. HL, DK, BC, and CL contributed to the conception of the experiments and supervising the research. HC contributed to the conception of the experiments, supervising the research, and writing and revising the manuscript.

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Correspondence to Hyung-Kyoon Choi.

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Lee, H., Noh, Y., Hong, SJ. et al. Photosynthetic pigment production and metabolic and lipidomic alterations in the marine cyanobacteria Synechocystis sp. PCC 7338 under various salinity conditions. J Appl Phycol 33, 197–209 (2021). https://doi.org/10.1007/s10811-020-02273-3

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  • DOI: https://doi.org/10.1007/s10811-020-02273-3

Keywords

  • Cyanobacteria
  • Synechocystis sp. PCC 7338
  • Salt stress
  • Pigments
  • Metabolic profile
  • Lipidomic profile