Phenotypic characterization of Synechocystis sp. PCC 6803 substrains reveals differences in sensitivity to abiotic stress

. 2017 ; 12 (12) : e0189130. [epub] 20171207

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29216280

Synechocystis sp. PCC 6803 is a widely used model cyanobacterium, whose substrains can vary on both genotype and phenotype levels. Previously described phenotypic variations include ability of mixotrophic growth, ability of movement on agar plates and variations in pigments composition or cell size. In this study, we report for the first time significant variation among Synechocystis substrains in complex cellular traits such as growth rate, photosynthesis efficiency, cellular dry weight and cellular composition (including protein or carbohydrates content). We also confirmed previously reported differences in cell size. Synechocystis cultures were cultivated in controlled environment of flat panel photobioreactors under red, blue and white light of intensities up to 790 μmol(photons) m-2 s-1, temperatures 23°C-60°C, input CO2 concentrations ranging from 400 to 15 000 ppm and in BG11 cultivation medium with and without addition of NaCl. Three Synechocystis substrains were used for the comparative experiments: GT-L, GT-B (Brno, CZ) and PCC-B (Brno, CZ). Growth rates of Synechocystis GT-B were inhibited under high intensities of red light (585-670 nm), and growth rates of both substrains GT-B and PCC-B were inhibited under photons of wavelengths 485-585 nm and 670-700 nm. Synechocystis GT-B was more sensitive to low temperatures than the other two tested substrains, and Synechocystis GT-L was sensitive to the presence of NaCl in the cultivation media. The results suggest that stress sensitivity of commonly used Synechocystis substrains can strongly vary, similarly as glucose tolerance or motility as reported previously. Our study further supports the previous statement that emphasizes importance of proper Synechocystis substrains selection and awareness of phenotypical differences among Synechocystis substrains which is crucial for comparative and reproducible research. This is highly relevant for studies related to stress physiology and development of sustainable biotechnological applications.

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Sarsekeyeva F, Zayadan BK, Usserbaeva A, Bedbenov VS, Sinetova MA, Los DA. Cyanofuels: Biofuels from cyanobacteria. Reality and perspectives. Photosynth Res. Springer Netherlands; 2015;125: 329–340. doi: 10.1007/s11120-015-0103-3 PubMed DOI

Wijffels RH, Kruse O, Hellingwerf KJ. Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol. 2013;24: 405–13. doi: 10.1016/j.copbio.2013.04.004 PubMed DOI

Kaneko T, Tanaka a, Sato S, Kotani H, Sazuka T, Miyajima N, et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. I. Sequence features in the 1 Mb region from map positions 64% to 92% of the genome. DNA Res. 1995;2: 153–166, 191–198. doi: 10.1093/dnares/2.4.153 PubMed DOI

Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, et al. 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. 1996;3: 109–136. doi: 10.1093/dnares/3.3.109 PubMed DOI

Grigorieva G, Shestakov S. Transformation in the cyanobacterium Synechocystis sp. 6803. FEMS Microbiol Lett. 1982;13: 367–370. Available: http://onlinelibrary.wiley.com/doi/10.1111/j.1574-6968.1982.tb08289.x/full DOI

Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev. 1971;35: 171–205. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=378380&tool=pmcentrez&rendertype=abstract PubMed PMC

Ikeuchi M, Tabata S. Synechocystis sp. PCC 6803—a useful tool in the study of the genetics of cyanobacteria. Photosynth Res. 2001;70: 73–83. doi: 10.1023/A:1013887908680 PubMed DOI

Tajima N, Sato S, Maruyama F, Kaneko T, Sasaki N V, Kurokawa K, et al. Genomic structure of the cyanobacterium Synechocystis sp. PCC 6803 strain GT-S. DNA Res. 2011;18: 393–9. doi: 10.1093/dnares/dsr026 PubMed DOI PMC

Morris J, Crawford T, Jeffs a, Stockwell P, Eaton-Rye J, Summerfield T. Whole genome re-sequencing of two “wild-type” strains of the model cyanobacterium Synechocystis sp. PCC 6803. New Zeal J Bot. Taylor & Francis; 2014;52: 36–47. doi: 10.1080/0028825X.2013.846267 DOI

Trautmann D, Voss B, Wilde A, Al-Babili S, Hess WR. Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Res. 2012;19: 435–48. doi: 10.1093/dnares/dss024 PubMed DOI PMC

Kanesaki Y, Shiwa Y, Tajima N, Suzuki M, Watanabe S, Sato N, et al. Identification of substrain-specific mutations by massively parallel whole-genome resequencing of Synechocystis sp. PCC 6803. DNA Res. 2012;19: 67–79. doi: 10.1093/dnares/dsr042 PubMed DOI PMC

Tichý M, Bečková M, Kopečná J, Noda J, Sobotka R, Komenda J. Strain of Synechocystis PCC 6803 with Aberrant Assembly of Photosystem II Contains Tandem Duplication of a Large Chromosomal Region. Front Plant Sci. 2016;7: 1–10. doi: 10.3389/fpls.2016.00648 PubMed DOI PMC

Ding Q, Chen G, Wang Y, Wei D. Identification of specific variations in a non-motile strain of cyanobacterium synechocystis sp. PCC 6803 originated from ATCC 27184 by whole genome resequencing. Int J Mol Sci. 2015;16: 24081–24093. doi: 10.3390/ijms161024081 PubMed DOI PMC

Zerulla K, Ludt K, Soppa J. The ploidy level of Synechocystis sp. PCC 6803 is highly variable and is influenced by growth phase and by chemical and physical external parameters. Microbiology. 2016;162: 730–739. doi: 10.1099/mic.0.000264 PubMed DOI

Morris JN, Eaton-Rye JJ, Summerfield TC. Phenotypic variation in wild-type substrains of the model cyanobacterium Synechocystis sp. PCC 6803. New Zeal J Bot. 2016; doi: 10.1080/0028825X.2016.1231124 DOI

Williams JGK. Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 1988;167: 766–778. doi: 10.1016/0076-6879(88)67088-1 DOI

Nedbal L, Trtílek M, Cervený J, Komárek O, Pakrasi HB. A photobioreactor system for precision cultivation of photoautotrophic microorganisms and for high-content analysis of suspension dynamics. Biotechnol Bioeng. 2008;100: 902–10. doi: 10.1002/bit.21833 PubMed DOI

ervený J, Šetlík I, Trtílek M, Nedbal L. Photobioreactor for cultivation and real-time, in-situ measurement of O2 and CO2 exchange rates, growth dynamics, and of chlorophyll fluorescence emission of photoautotrophic microorganisms. Eng Life Sci. 2009;9: 247–253. doi: 10.1002/elsc.200800123 DOI

Zavřel T, Sinetova MA, Búzová D, Literáková P, Červený J. Characterization of a model cyanobacterium Synechocystis sp. PCC 6803 autotrophic growth in a flat-panel photobioreactor. Eng Life Sci. 2015;15: 122–132. doi: 10.1002/elsc.201300165 DOI

Sinetova MA, Červený J, Zavřel T, Nedbal L. On the dynamics and constraints of batch culture growth of the cyanobacterium Cyanothece sp. ATCC 51142. J Biotechnol. 2012;162: 148–55. doi: 10.1016/j.jbiotec.2012.04.009 PubMed DOI

Zavřel T, Sinetova MA, Červený J. Measurement of Chlorophyll a and Carotenoids Concentration in Cyanobacteria. bio-protocol. 2015;5: 1–5. Available: http://www.bio-protocol.org/e1467 PubMed

Bennett a, Bogorad L. Complementary chromatic adaption in a filamentous blue-green alga. JCellBiol. 1973;58: 419–435. PubMed PMC

Dubois M, Gilles K a, Ton JKH, Rebers P a, Smith F. Colorimetric Method for Determination of Sugars and Related Substances. Anal Chem. 1956;28: 350–356. doi: 10.1021/ac60111a017 DOI

Hagemann M. Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev. 2011;35: 87–123. doi: 10.1111/j.1574-6976.2010.00234.x PubMed DOI

Hihara Y, Ikeuchi M. Mutation in a novel gene required for photomixotrophic growth leads to enhanced photoautotrophic growth of Synechocystis sp. PCC 6803. Photosynth Res. 1997;53: 243–252. Available: http://dx.doi.org/10.1023/A:1005879905365 DOI

Kahlon S, Beeri K, Ohkawa H, Hihara Y, Murik O, Suzuki I, et al. A putative sensor kinase, Hik31, is involved in the response of Synechocystis sp. strain PCC 6803 to the presence of glucose. Microbiology. 2006;152: 647–655. doi: 10.1099/mic.0.28510-0 PubMed DOI

Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Govindjee, et al. The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta—Bioenerg. 2012;1817: 1237–1247. doi: 10.1016/j.bbabio.2012.02.024 PubMed DOI

Joseph A, Aikawa S, Sasaki K, Matsuda F, Hasunuma T, Kondo A. Increased biomass production and glycogen accumulation in apcE gene deleted Synechocystis sp. PCC 6803. AMB Express. 2014;4: 17 doi: 10.1186/s13568-014-0017-z PubMed DOI PMC

Gründel M, Scheunemann R, Lockau W, Zilliges Y. Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology. 2012;158: 3032–43. doi: 10.1099/mic.0.062950-0 PubMed DOI

Gründel M, Scheunemann R, Lockau W, Zilliges Y. Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiol (United Kingdom). 2012;158: 3032–3043. doi: 10.1099/mic.0.062950–0 PubMed DOI

Touloupakis E, Cicchi B, Torzillo G. A bioenergetic assessment of photosynthetic growth of Synechocystis sp. PCC 6803 in continuous cultures. Biotechnol Biofuels. BioMed Central; 2015;8: 133 doi: 10.1186/s13068-015-0319-7 PubMed DOI PMC

Kirilovsky D, Kaňa R, Prášil O. Mechanisms Modulating Energy Arriving at Reaction Centers in Cyanobacteria. Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. 2014. doi: 10.1007/978-94-017-9032-1 DOI

Mironov KS, Los DA. Light Regulation of Cold Stress Responses in Synechocystis Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2016. pp. 881–889. doi: 10.1002/9781119004813.ch86 DOI

Sinetova MA, Los DA. Lessons from cyanobacterial transcriptomics: Universal genes and triggers of stress responses. Mol Biol. 2016;50: 606–614. doi: 10.1134/S0026893316040117 PubMed DOI

Wada H, Murata N. Temperature-induced Changes in the Fatty Acid Composition of the Cyanobacterium, Synechocystis PCC 6803. Plant Physiol. 1990; 1062–1069. PubMed PMC

Dilley R a, Nishiyama Y, Gombos Z, Murata N. Bioenergetic responses of Synechocystis 6803 fatty acid desaturase mutants at low temperatures. J Bioenerg Biomembr. 2001;33: 135–41. Available: http://www.ncbi.nlm.nih.gov/pubmed/11456219 PubMed

Nanjo Y, Mizusawa N, Wada H, Slabas AR, Hayashi H, Nishiyama Y. Synthesis of fatty acids de novo is required for photosynthetic acclimation of Synechocystis sp. PCC 6803 to high temperature. Biochim Biophys Acta. Elsevier B.V.; 2010;1797: 1483–90. doi: 10.1016/j.bbabio.2010.03.014 PubMed DOI

Sinetova MA, Los DA. New insights in cyanobacterial cold stress responses: Genes, sensors, and molecular triggers. Biochim Biophys Acta—Gen Subj. Elsevier B.V.; 2016;1860: 2391–2403. doi: 10.1016/j.bbagen.2016.07.006 PubMed DOI

Kreslavski VD, Fomina IR, Los DA, Carpentier R, Kuznetsov V V., Allakhverdiev SI. Red and near infra-red signaling: Hypothesis and perspectives. J Photochem Photobiol C Photochem Rev. 2012;13: 190–203. doi: 10.1016/j.jphotochemrev.2012.01.002 DOI

Červený J, Sinetova MA, Zavřel T, Los DA. Mechanisms of high temperature resistance of Synechocystis sp. PCC 6803: An Impact of histidine kinase 34. Life. 2015;5: 676–699. doi: 10.3390/life5010676 PubMed DOI PMC

Sheng J, Kim HW, Badalamenti JP, Zhou C, Sridharakrishnan S, Krajmalnik-Brown R, et al. Effects of temperature shifts on growth rate and lipid characteristics of Synechocystis sp. PCC6803 in a bench-top photobioreactor. Bioresour Technol. Elsevier Ltd; 2011;102: 11218–25. doi: 10.1016/j.biortech.2011.09.083 PubMed DOI

Inoue N, Taira Y, Emi T, Yamane Y, Kashino Y, Koike H, et al. Acclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol. 2001;42: 1140–8. Available: http://www.ncbi.nlm.nih.gov/pubmed/11673630 PubMed

Fang F, Barnum SR. The heat shock gene, htpG, and thermotolerance in the cyanobacterium, Synechocystis sp. PCC 6803. Curr Microbiol. 2003;47: 341–346. doi: 10.1007/s00284-002-4015-z PubMed DOI

Huflejt ME, Tremolieres A, Pineau B, Lang JK, Hatheway J, Packer L. Changes in membrane lipid composition during saline growth of the fresh water cyanobacterium Synechococcus 6311. Plant Physiol. 1990;94: 1512–1521. doi: 10.1104/pp.94.4.1512 PubMed DOI PMC

Pade N, Hagemann M. Salt Acclimation of Cyanobacteria and Their Application in Biotechnology. Life. 2014;5: 25–49. doi: 10.3390/life5010025 PubMed DOI PMC

Marin K, Kanesaki Y, Los D a, Murata N, Suzuki I, Hagemann M. Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803. Plant Physiol. 2004;136: 300–329. doi: 10.1104/pp.104.045047.3290 PubMed DOI PMC

Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, et al. Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics. 2006;6: 2733–2745. doi: 10.1002/pmic.200500538 PubMed DOI

Torrecilla I, Leganes F, Bonilla I, Fernandez-pinas F. Calcium transits in response to salinity and osmotic stress in the nitrogen-fix cyanobacterium Anabaena sp. PCC7120, expressing cytosolic apoaequorin. Plant Cell Environ. 2001;24: 641–648.

Nazarenko L V., Andreev IM, Lyukevich AA, Pisareva T V., Los DA. Calcium release from Synechocystis cells induced by depolarization of the plasma membrane: MscL as an outward Ca2+ channel. Microbiology. 2003;149: 1147–1153. doi: 10.1099/mic.0.26074-0 PubMed DOI

Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology. 1979;111: 1–61. doi: 10.1099/00221287-111-1-1 DOI

Platt T, Gallegos CL, Harrison WG. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res. 1980;38: 687–701.

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