Mechanisms of High Temperature Resistance of Synechocystis sp. PCC 6803: An Impact of Histidine Kinase 34
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
25738257
PubMed Central
PMC4390874
DOI
10.3390/life5010676
PII: life5010676
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
Synechocystis sp. PCC 6803 is a widely used model cyanobacterium for studying responses and acclimation to different abiotic stresses. Changes in transcriptome, proteome, lipidome, and photosynthesis in response to short term heat stress are well studied in this organism, and histidine kinase 34 (Hik34) is shown to play an important role in mediating such response. Corresponding data on long term responses, however, are fragmentary and vary depending on parameters of experiments and methods of data collection, and thus are hard to compare. In order to elucidate how the early stress responses help cells to sustain long-term heat stress, as well as the role of Hik34 in prolonged acclimation, we examined the resistance to long-term heat stress of wild-type and ΔHik34 mutant of Synechocystis. In this work, we were able to precisely control the long term experimental conditions by cultivating Synechocystis in automated photobioreactors, measuring selected physiological parameters within a time range of minutes. In addition, morphological and ultrastructural changes in cells were analyzed and western blotting of individual proteins was used to study the heat stress-affected protein expression. We have shown that the majority of wild type cell population was able to recover after 24 h of cultivation at 44 °C. In contrast, while ΔHik34 mutant cells were resistant to heat stress within its first hours, they could not recover after 24 h long high temperature treatment. We demonstrated that the early induction of HspA expression and maintenance of high amount of other HSPs throughout the heat incubation is critical for successful adaptation to long-term stress. In addition, it appears that histidine kinase Hik34 is an essential component for the long term high temperature resistance.
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Zavřel T., Literáková P., Búzová D., Sinetova M.A., Červený J. Characterization of a model cyanobacterium Synechocystis sp. PCC 6803 autotrophic growth in a flat-panel photobioreactor. Eng. Life Sci. 2014;15:122–132. doi: 10.1002/elsc.201300165. DOI
Suzuki I., Kanesaki Y., Hayashi H., Hall J.J., Simon W.J., Slabas A.R., Murata N. The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol. 2005;138:1409–1421. doi: 10.1104/pp.104.059097. PubMed DOI PMC
Slabas A.R., Suzuki I., Murata N., Simon W.J., Hall J.J. Proteomic analysis of the heat shock response in Synechocystis PCC 6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics. 2006;6:845–864. doi: 10.1002/pmic.200500196. PubMed DOI
Singh A.K., Summerfield T.C., Li H., Sherman L.A. The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol. 2006;186:273–286. doi: 10.1007/s00203-006-0138-0. PubMed DOI
Tuominen I., Pollari M., von Wobeser A.E., Tyystjarvi E., Ibelings B.W., Matthijs H.C., Tyystjarvi T. Sigma factor SigC is required for heat acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803. FEBS Lett. 2008;582:346–350. doi: 10.1016/j.febslet.2007.12.030. PubMed DOI
Tuominen I., Pollari M., Tyystjarvi E., Tyystjarvi T. The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 2006;580:319–323. doi: 10.1016/j.febslet.2005.11.082. PubMed DOI
Aminaka R., Taira Y., Kashino Y., Koike H., Satoh K. Acclimation to the growth temperature and thermosensitivity of photosystem II in a mesophilic cyanobacterium, Synechocystis sp. PCC 6803. Plant Cell Physiol. 2006;47:1612–1621. doi: 10.1093/pcp/pcl024. PubMed DOI
Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta. 2007;1767:414–421. doi: 10.1016/j.bbabio.2006.11.019. PubMed DOI
Balogi Z., Török Z., Balogh G., Jósvay K., Shigapova N., Vierling E., Vígh L., Horváth I. “Heat shock lipid” in cyanobacteria during heat/light-acclimation. Arch. Biochem. Biophys. 2005;436:346–354. doi: 10.1016/j.abb.2005.02.018. PubMed DOI
Inoue N., Taira Y., Emi T., Yamane Y., Kashino Y., Koike H., Satoh K. Acclimation to growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mezophilic cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 2001;42:1140–1148. doi: 10.1093/pcp/pce147. PubMed DOI
Török Z., Goloubinoff P., Horváth I., Tsvetkova N.M., Glatz A., Balogh G., Varvasovszki V., Los D.A., Vierling E., Crowe J.H., et al. Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc. Natl. Acad. Sci. USA. 2001;98:3098–3103. doi: 10.1073/pnas.051619498. PubMed DOI PMC
Nakamoto H., Suzuki M., Kojima K. Targeted inactivation of the hrcA repressor gene in cyanobacteria. FEBS Lett. 2003;549:57–62. doi: 10.1016/S0014-5793(03)00768-3. PubMed DOI
Lee S., Owen H.A., Prochaska D.J., Barnum S.R. HSP16.6 is involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium, Synechocystis sp. PCC 6803. Curr. Microbiol. 2000;40:283–287. doi: 10.1007/s002849910056. PubMed DOI
Fang F., Barnum S.R. 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
Kaczmarzyk D., Anfelt J., Sarnegrim A., Hudson E.P. Overexpression of sigma factor SigB improves temperature and butanol tolerance of Synechocystis sp. PCC 6803. J. Biotechnol. 2014;182–183:54–60. doi: 10.1016/j.jbiotec.2014.04.017. PubMed DOI
Sheng J., Kim H.W., Badalamenti J.P., Zhou C., Sridharakrishnan S., Krajmalnik-Brown R., Rittmann B.E., Vannela R. Effects of temperature shifts on growth rate and lipid characteristics of Synechocystis sp. PCC 6803 in a bench-top photobioreactor. Bioresour. Technol. 2011;102:11218–11225. doi: 10.1016/j.biortech.2011.09.083. PubMed DOI
Suzuki I., Simon W.J., Slabas A.R. The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. J. Exp. Bot. 2006;57:1573–1578. doi: 10.1093/jxb/erj148. PubMed DOI
Lehel C., Wada H., Kovács E., Török Z., Gombos Z., Horváth I., Murata N., Vigh L. Heat shock protein synthesis of the cyanobacterium Synechocystis PCC 6803: Purification of the GroEL-related chaperonin. Plant Mol. Biol. 1992;18:327–336. doi: 10.1007/BF00034959. PubMed DOI
Krishna P.S., Rani B.R., Mohan M.K., Suzuki I., Shivaji S., Prakash J.S. A novel transcriptional regulator, Sll1130, negatively regulates heat-responsive genes in Synechocystis sp. PCC 6803. Biochem. J. 2013;449:751–760. doi: 10.1042/BJ20120928. PubMed DOI
Kortmann J., Sczodrok S., Rinnenthal J., Schwalbe H., Narberhaus F. Translation on demand by a simple RNA-based thermosensor. Nucleic Acids Res. 2011;39:2855–2868. doi: 10.1093/nar/gkq1252. PubMed DOI PMC
Asadulghani, Suzuki Y., Nakamoto H. Light plays a key role in the modulation of heat shock response in the cyanobacterium Synechocystis sp. PCC 6803. Biochem. Biophys. Res. Commun. 2003;306:872–879. doi: 10.1016/S0006-291X(03)01085-4. PubMed DOI
Los D.A., Suzuki I., Zinchenko V.V., Murata N. Stress responses in Synechocystis: Regulated genes and regulatory systems. In: Herrero A., Flores E., editors. The Cyanobacteria: Molecular Biology, Genomics and Evolution. Caister Academic Press; Norfolk, UK: 2008. pp. 117–157.
Murata N., Suzuki I. Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J. Exp. Bot. 2006;57:235–247. doi: 10.1093/jxb/erj005. PubMed DOI
Ashby M.K., Houmard J. Cyanobacterial two-component proteins: Structure, diversity, distribution, and evolution. Microbiol. Mol. Biol. Rev. 2006;70:472–509. doi: 10.1128/MMBR.00046-05. PubMed DOI PMC
Marin K., Suzuki I., Yamaguchi K., Ribbeck K., Yamamoto H., Kanesaki Y., Hagemann M., Murata N. Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc. Natl. Acad. Sci. USA. 2003;100:9061–9066. doi: 10.1073/pnas.1532302100. PubMed DOI PMC
Hihara Y., Sonoike K., Kanehisa M., Ikeuchi M. DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. Strain PCC 6803. J. Bacteriol. 2003;185:1719–1725. doi: 10.1128/JB.185.5.1719-1725.2003. PubMed DOI PMC
Paithoonrangsarid K., Shumskaya M.A., Kanesaki Y., Satoh S., Tabata S., Los D.A., Zinchenko V.V., Hayashi H., Tanticharoen M., Suzuki I., et al. Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J. Biol. Chem. 2004;279:53078–53086. doi: 10.1074/jbc.M410162200. PubMed DOI
Shumskaya M.A., Paithoonrangsarid K., Kanesaki Y., Los D.A., Zinchenko V.V., Tanticharoen M., Suzuki I., Murata N. Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J. Biol. Chem. 2005;280:21531–21538. doi: 10.1074/jbc.M412174200. PubMed DOI
Kanesaki Y., Yamamoto H., Paithoonrangsarid K., Shumskaya M., Suzuki I., Hayashi H., Murata N. Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J. 2007;49:313–324. doi: 10.1111/j.1365-313X.2006.02959.x. PubMed DOI
Rowland J.G., Pang X., Suzuki I., Murata N., Simon W.J., Slabas A.R. Identification of components associated with thermal acclimation of photosystem II in Synechocystis sp. PCC 6803. PLoS One. 2010;5 doi: 10.1371/journal.pone.0010511. PubMed DOI PMC
Stanier R.Y., Kunisawa R., Mandel M., Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales) Bacteriol. Rev. 1971;35:171–205. PubMed PMC
Nedbal L., Trtílek M., Červený J., Komárek O., Pakrasi H.B. A photobioreactor system for precision cultivation of photoautotrophic microorganisms and for high-content analysis of suspension dynamics. Biotechnol. Bioeng. 2008;100:902–910. doi: 10.1002/bit.21833. PubMed DOI
Sinetova M.A., 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;162:148–155. doi: 10.1016/j.jbiotec.2012.04.009. PubMed DOI
Markelova A.G., Vladimirova M.G., Kuptsova E.S. A comparison of cytochemical methods for the rapid evaluation of microalgal viability. Russ. J. Plant Physiol. 2000;47:815–819. doi: 10.1023/A:1026619514661. DOI
Guilbault G.G., Kramer D.N. Fluorometric determination of lipase, acylase, alpha-, and gamma-chymotrypsin and inhibitors of these enzymes. Anal. Chem. 1964;36:409–412. doi: 10.1021/ac60208a052. DOI
Reynolds E.S. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 1963;17:208–212. doi: 10.1083/jcb.17.1.208. PubMed DOI PMC
Li H., Sherman L.A. A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 2000;182:4268–4277. doi: 10.1128/JB.182.15.4268-4277.2000. PubMed DOI PMC
Allakhverdiev S.I., Kreslavski V.D., Klimov V.V., Los D.A., Carpentier R., Mohanty P. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 2008;98:541–550. doi: 10.1007/s11120-008-9331-0. PubMed DOI
Inoue N., Emi T., Yamane Y., Kashino Y., Koike H., Satoh K. Effects of high-temperature treatments on a thermophilic cyanobacterium Synechococcus vulcanus. Plant Cell Physiol. 2000;41:515–522. doi: 10.1093/pcp/41.4.515. PubMed DOI
Stoitchkova K., Zsiros O., Jávorfi T., Páli T., Andreeva A., Gombos Z., Garab G. Heat- and light-induced reorganizations in the phycobilisome antenna of Synechocystis sp. PCC 6803. Thermo-optic effect. Biochim. Biophys. Acta Bioenerg. 2007;1767:750–756. doi: 10.1016/j.bbabio.2007.03.002. PubMed DOI
Horvath I., Glatz A., Nakamoto H., Mishkind M.L., Munnik T., Saidi Y., Goloubinoff P., Harwood J.L., Vigh L. Heat shock response in photosynthetic organisms: Membrane and lipid connections. Prog. Lipid Res. 2012;51:208–220. doi: 10.1016/j.plipres.2012.02.002. PubMed DOI
Van de Meene A.L., Hohmann-Marriott M., Vermaas W.J., Roberson R. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 2006;184:259–270. doi: 10.1007/s00203-005-0027-y. PubMed DOI
Trautner C., Vermaas W.F. The sll1951 gene encodes the surface layer protein of Synechocystis sp. strain PCC 6803. J. Bacteriol. 2013;195:5370–5380. doi: 10.1128/JB.00615-13. PubMed DOI PMC
Hall J.J. Ph.D. Thesis. Durham University; Durham, UK: 2005. Proteomic Analysis of the Heat Shock and Acclimation Responses of Cyanobacteria.
Sakthivel K., Watanabe T., Nakamoto H. A small heat-shock protein confers stress tolerance and stabilizes thylakoid membrane proteins in cyanobacteria under oxidative stress. Arch. Microbiol. 2009;191:319–328. doi: 10.1007/s00203-009-0457-z. PubMed DOI
Lee S., Prochaska D.J., Fang F., Barnum S.R. A 16.6-kilodalton protein in the cyanobacterium Synechocystis sp. PCC 6803 plays a role in the heat shock response. Curr. Microbiol. 1998;37:403–407. doi: 10.1007/s002849900400. PubMed DOI
Varvasovszki V., Glatz A., Shigapova N., Jósvay K., Vígh L., Horváth I. Only one dnaK homolog, dnaK2, is active transcriptionally and is essential in Synechocystis. Biochem. Biophys. Res. Commun. 2003;305:641–648. doi: 10.1016/S0006-291X(03)00822-2. PubMed DOI
Kovács E., van der Vies S.M., Glatz A., Török Z., Varvasovszki V., Horváth I., Vígh L. The chaperonins of Synechocystis PCC 6803 differ in heat inducibility and chaperone activity. Biochem. Biophys. Res. Commun. 2001;289:908–915. doi: 10.1006/bbrc.2001.6083. PubMed DOI
Srivastava R., Pisareva T., Norling B. Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803. Proteomics. 2005;5:4905–4916. doi: 10.1002/pmic.200500111. PubMed DOI
Tsvetkova N.M., Horvath I., Torok Z., Wolkers W.F., Balogi Z., Shigapova N., Crowe L.M., Tablin F., Vierling E., Crowe J.H., et al. Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. USA. 2002;99:13504–13509. doi: 10.1073/pnas.192468399. PubMed DOI PMC
Nitta K., Suzuki N., Honma D., Kaneko Y., Nakamoto H. Ultrastructural stability under high temperature or intensive light stress conferred by a small heat shock protein in cyanobacteria. FEBS Lett. 2005;579:1235–1242. doi: 10.1016/j.febslet.2004.12.095. PubMed DOI
Rupprecht E., Gathmann S., Fuhrmann E., Schneider D. Three different DnaK proteins are functionally expressed in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology. 2007;153:1828–1841. doi: 10.1099/mic.0.2007/005876-0. PubMed DOI
Asadulghani, Nitta K., Kaneko Y., Kojima K., Fukuzawa H., Kosaka H., Nakamoto H. Comparative analysis of the hspA mutant and wild-type Synechocystis sp. strain PCC 6803 under salt stress: Evaluation of the role of hspA in salt-stress management. Arch. Microbiol. 2004;182:487–497. doi: 10.1007/s00203-004-0733-x. PubMed DOI
Mansilla M., Banchio C., de Mendoza D. Signalling pathways controlling fatty acid desaturation. In: Quinn P., Wang X., editors. Lipids in Health and Disease. Volume 49. Springer; Dordrecht, the Netherlands: 2008. pp. 71–99. PubMed
Sakayori T., Shiraiwa Y., Suzuki I. A Synechocystis homolog of SipA protein, Ssl3451, enhances the activity of the histidine kinase Hik33. Plant Cell Physiol. 2009;50:1439–1448. doi: 10.1093/pcp/pcp089. PubMed DOI
Towards a quantitative assessment of inorganic carbon cycling in photosynthetic microorganisms