The Role of FtsH Complexes in the Response to Abiotic Stress in Cyanobacteria
Jazyk angličtina Země Japonsko Médium print
Typ dokumentu časopisecké články, přehledy
Grantová podpora
24-10227S
Grantová Agentura Ceské Republiky
P JAC project. No. CZ.02.01.01/00/22_008/0004624
Czech Ministry of Education, Sports and Youth
854126
H2020 European Research Council
24-10227S
Grantová Agentura Ceské Republiky
P JAC project. No. CZ.02.01.01/00/22_008/0004624
Czech Ministry of Education, Sports and Youth
854126
H2020 European Research Council
PubMed
38619128
PubMed Central
PMC11287208
DOI
10.1093/pcp/pcae042
PII: 7645829
Knihovny.cz E-zdroje
- Klíčová slova
- Cyanobacteria, FtsH, Nutrient stress, Photodamage, Photosystem,
- MeSH
- bakteriální proteiny * metabolismus genetika MeSH
- fyziologický stres * MeSH
- proteasy závislé na ATP metabolismus genetika MeSH
- sinice * metabolismus fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- bakteriální proteiny * MeSH
- proteasy závislé na ATP MeSH
FtsH proteases (FtsHs) belong to intramembrane ATP-dependent metalloproteases which are widely distributed in eubacteria, mitochondria and chloroplasts. The best-studied roles of FtsH in Escherichia coli include quality control of membrane proteins, regulation of response to heat shock, superoxide stress and viral infection, and control of lipopolysaccharide biosynthesis. While heterotrophic bacteria mostly contain a single indispensable FtsH complex, photosynthetic cyanobacteria usually contain three FtsH complexes: two heterocomplexes and one homocomplex. The essential cytoplasmic FtsH1/3 most probably fulfills a role similar to other bacterial FtsHs, whereas the thylakoid FtsH2/3 heterocomplex and FtsH4 homocomplex appear to maintain the photosynthetic apparatus of cyanobacteria and optimize its functionality. Moreover, recent studies suggest the involvement of all FtsH proteases in a complex response to nutrient stresses. In this review, we aim to comprehensively evaluate the functions of the cyanobacterial FtsHs specifically under stress conditions with emphasis on nutrient deficiency and high irradiance. We also point to various unresolved issues concerning FtsH functions, which deserve further attention.
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Adam Z., Halperin T., Itzhaki H., Lindahl M., Ostersetzer O. (1998) The proteolytic machinery of chloroplasts: homologues of bacterial proteases. In Photosynthesis: Mechanisms and Effects. Edited by Garab, G. pp. 1871–1876. Springer, Dordrecht.
Adam Z., Rudella A. and van Wijk K.J. (2006) Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr. Opin. Cell Biol. 9: 234–240. PubMed
Arends J., Thomanek N., Kuhlmann K., Marcus K. and Narberhaus F. (2016) In vivo trapping of FtsH substrates by label-free quantitative proteomics. Proteomics 16: 3161–3172. PubMed
Bečková M., Gardian Z., Yu J.F., Koník P., Nixon P.J. and Komenda J. (2017a) Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp PCC 6803 to high light. Mol. Plant 10: 62–72. PubMed
Bečková M., Yu J., Krynická V., Kozlo A., Shao S., Koník P., et al. (2017b) Structure of Psb29/Thf1 and its association with the FtsH protease complex involved in photosystem II repair in cyanobacteria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372: 20160394. PubMed PMC
Boehm M., Nield J., Zhang P., Aro E.M., Komenda J. and Nixon P.J. (2009) Structural and mutational analysis of band 7 proteins in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 191: 6425–6435. PubMed PMC
Boehm M., Yu J., Krynická V., Barker M., Tichý M., Komenda J., et al. (2012) Subunit organization of a Synechocystis hetero-oligomeric thylakoid FtsH complex involved in photosystem II repair. Plant Cell 24: 3669–3683. PubMed PMC
Bonisteel E.M., Turner B.E., Murphy C.D., Melanson J.R., Duff N.M., Beardsall B.D., et al. (2018) Strain specific differences in rates of photosystem II repair in picocyanobacteria correlate to differences in FtsH protein levels and isoform expression patterns. PLoS One 13: e0209115. PubMed PMC
Bryant J.A., Sellars L.E., Busby S.J. and Lee D.J. (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res. 42: 11383–11392. PubMed PMC
Burnap R.L., Hagemann M. and Kaplan A. (2015) Regulation of CO2 concentrating mechanism in cyanobacteria. Life 5: 348–371. PubMed PMC
Dühring U., Axmann I.M., Hess W.R. and Wilde A. (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc. Natl. Acad. Sci. U.S.A. 103: 7054–7058. PubMed PMC
Espinosa J., Forchhammer K. and Contreras A. (2007) Role of the Synechococcus PCC 7942 nitrogen regulator protein PipX in NtcA-controlled processes. Microbiology 153: 711–718. PubMed
Espinosa J., Rodriguez-Mateos F., Salinas P., Lanza V.F., Dixon R., de la Cruz F., et al. (2014) PipX, the coactivator of NtcA, is a global regulator in cyanobacteria. Proc. Natl. Acad. Sci. U.S.A. 111: E2423–E2430. PubMed PMC
Ferro M., Brugière S., Salvi D., Seigneurin-Berny D., Court M., Moyet L., et al. (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteom. 9: 1063–1084. PubMed PMC
Ferro M., Salvi D., Brugière S., Miras S., Kowalski S., Louwagie M., et al. (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell. Proteom. 2: 325–345. PubMed
Fillat M.F. (2014) The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch. Biochem. Biophys. 546: 41–52. PubMed
Fokina O., Herrmann C. and Forchhammer K. (2011) Signal-transduction protein PII from Synechococcus elongatus PCC 7942 senses low adenylate energy charge in vitro. Biochem. J. 440: 147–156. PubMed
Forchhammer K., Huergo L.F. and Huergo L.F. (2022) New views on PII signaling: from nitrogen sensing to global metabolic control. Trends Microbiol. 30: 722–735. PubMed
Forchhammer K. and Selim K.A. (2020) Carbon/nitrogen homeostasis control in cyanobacteria. FEMS Microbiol. Rev. 44: 33–53. PubMed PMC
Fu W., Cui Z., Guo J., Cui X., Han G., Zhu Y., et al. (2023) Immunophilin CYN28 is required for accumulation of photosystem II and thylakoid FtsH protease in Chlamydomonas. Plant Physiol. 191: 1002–1016. PubMed PMC
Gómez-Baena G., Rangel O.A., López-Lozano A., García-Fernández J.M. and Diez J. (2009) Stress responses in Prochlorococcus MIT9313 vs. SS120 involve differential expression of genes encoding proteases ClpP, FtsH and Lon. Res. Microbiol. 160: 567–575. PubMed
Gonzalez A., Espinosa Angarica V., Sancho J. and Fillat M.F. (2014) The FurA regulon in Anabaena sp PCC 7120: in silico prediction and experimental validation of novel target genes. Nucleic Acids Res. 42: 4833–4846. PubMed PMC
Gonzalez A., Teresa Bes M., Luisa Peleato M., Fillat M.F. and Hess W.R. (2016) Expanding the role of FurA as essential global regulator in cyanobacteria. Plos One 11: e0151384. PubMed PMC
Hagemann M., Song S., Brouwer E.-M. (2021) Inorganic carbon assimilation in cyanobacteria: mechanisms, regulation, and engineering. In Cyanobacteria Biotechnology. Edited by Hudson, P., Lee, S.Y. and Nielsen, J. pp. 1–31. Wiley-Blackwell, Weinheim.
Huergo L.F. and Dixon R. (2015) The emergence of 2-oxoglutarate as a master regulator metabolite. Microbiol. Mol. Biol. Rev. 79: 419–435. PubMed PMC
Ito K. and Akiyama Y. (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 59: 211–231. PubMed
Jackson P.J., Hitchcock A., Brindley A.A., Dickman M.J. and Hunter C.N. (2023) Absolute quantification of cellular levels of photosynthesis-related proteins in Synechocystis sp. PCC 6803. Photosynth. Res. 155: 219–245. PubMed PMC
Janska H., Kwasniak M. and Szczepanowska J. (2013) Protein quality control in organelles – AAA/FtsH story. Biochim. Biophys. Acta 1833: 381–387. PubMed
Jia A., Zheng Y., Chen H. and Wang Q. (2021) Regulation and functional complexity of the chlorophyll-binding protein IsiA. Front. Microbiol. 12: 774107. PubMed PMC
Kaplan A., Ronen-Tarazi M., Tchernov D., Bonfil D.J., Zer H., Schatz D., et al. (1999) The inorganic carbon-concentrating mechanism of cyanobacteria. In Phototrophic Prokaryotes Edited by Peschek, G.A., Löffelhardt, W. and Schmetterer, G. pp. 561–571. Springer, Boston.
Kato Y., Kuroda H., Ozawa S.I., Saito K., Dogra V., Scholz M., et al. (2023) Characterization of tryptophan oxidation affecting D1 degradation by FtsH in the photosystem II quality control of chloroplasts. eLife 12: RP88822. PubMed PMC
Kato Y. and Sakamoto W. (2018) FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. Front. Plant Sci. 9: 855. PubMed PMC
Kato Y. and Sakamoto W. (2019) Phosphorylation of the chloroplastic metalloprotease FtsH in Arabidopsis characterized by Phos-Tag SDS-PAGE. Front. Plant Sci. 10: 1080. PubMed PMC
Keren N., Ohkawa H., Welsh E.A., Liberton M. and Pakrasi H.B. (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell 17: 2768–2781. PubMed PMC
Kihara A., Akiyama Y. and Ito K. (1996) A protease complex in the Escherichia coli plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY. Embo J. 15: 6122–6131. PubMed PMC
Klahn S., Orf I., Schwarz D., Matthiessen J.K., Kopka J., Hess W.R., et al. (2015) Integrated transcriptomic and metabolomic characterization of the low-carbon response using an ndhR mutant of Synechocystis sp. PCC 6803. Plant Physiol. 169: 1540–1556. PubMed PMC
Kloft N. and Forchhammer K. (2005) Signal transduction protein PII phosphatase PphA is required for light-dependent control of nitrate utilization in Synechocystis sp. strain PCC 6803. J. Bacteriol. 187: 6683–6690. PubMed PMC
Knoppová J., Sobotka R., Yu J., Bečková M., Pilný J., Trinugroho J.P., et al. (2022) Assembly of D1/D2 complexes of photosystem II: binding of pigments and a network of auxiliary proteins. Plant Physiol. 189: 790–804. PubMed PMC
Komenda J., Barker M., Kuviková S., de Vries R., Mullineaux C.W., Tichý M., et al. (2006) The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp PCC 6803. J. Biol. Chem. 281: 1145–1151. PubMed
Komenda J., Knoppová J., Krynická V., Nixon P.J. and Tichý M. (2010) Role of FtsH2 in the repair of photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster. Biochim. Biophys. Acta 1797: 566–575. PubMed
Komenda J. and Sobotka R. (2016) Cyanobacterial high-light-inducible proteins – protectors of chlorophyll-protein synthesis and assembly. Biochim. Biophys. Acta 1857: 288–295. PubMed
Komenda J., Tichý M., Prášil O., Knoppová J., Kuviková S., de Vries R., et al. (2007) The exposed N-terminal tail of the D1 subunit is required for rapid D1 degradation during photosystem II repair in Synechocystis sp PCC 6803. Plant Cell 19: 2839–2854. PubMed PMC
Koník P., Skotnicová P., Gupta S., Tichý M., Sharma S., Komenda J., et al. (2024) The cyanobacterial FtsH4 protease controls accumulation of protein factors involved in the biogenesis of photosystem I. Biochim. Biophys. Acta 1865: 149017. PubMed
Kopečná J., Komenda J., Bučinská L. and Sobotka R. (2012) Long-term acclimation of the cyanobacterium Synechocystis sp PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric photosystem I. Plant Physiol. 160: 2239–2250. PubMed PMC
Kopf M., Klaehn S., Scholz I., Matthiessen J.K.F., Hess W.R. and Voss B. (2014) Comparative analysis of the primary transcriptome of Synechocystis sp PCC 6803. DNA Res 21: 527–539. PubMed PMC
Krynická V., Georg J., Jackson P.J., Dickman M.J., Hunter C.N., Futschik M.E., et al. (2019) Depletion of the FtsH1/3 proteolytic complex suppresses the nutrient stress response in the cyanobacterium Synechocystis sp strain PCC 6803. Plant Cell 31: 2912–2928. PubMed PMC
Krynická V., Shao S., Nixon P.J. and Komenda J. (2015) Accessibility controls selective degradation of photosystem II subunits by FtsH protease. Nat. Plants 1: 15168. PubMed
Krynická V., Skotnicová P., Jackson P.J., Barnett S., Yu J., Wysocka A., et al. (2023) FtsH4 protease controls biogenesis of the PSII complex by dual regulation of high light-inducible proteins. Plant Commun. 4: 100502. PubMed PMC
Krynická V., Tichý M., Krafl J., Yu J., Kaňa R., Boehm M., et al. (2014) Two essential FtsH proteases control the level of the Fur repressor during iron deficiency in the cyanobacterium Synechocystis sp PCC 6803. Mol. Microbiol. 94: 609–624. PubMed
Kurisu G., Zhang H., Smith J.L. and Cramer W.A. (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302: 1009–1014. PubMed
Langklotz S., Baumann U. and Narberhaus F. (2012) Structure and function of the bacterial AAA protease FtsH. Biochim. Biophys. Acta 1823: 40–48. PubMed
Linhartová M., Bučinská L., Halada P., Ječmen T., Šetlík J., Komenda J., et al. (2014) Accumulation of the Type IV prepilin triggers degradation of SecY and YidC and inhibits synthesis of photosystem II proteins in the cyanobacterium Synechocystis PCC 6803. Mol. Microbiol. 93: 1207–1223. PubMed
Llácer J.L., Espinosa J., Castells M.A., Contreras A., Forchhammer K. and Rubio V. (2010) Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. Proc. Natl. Acad. Sci. U.S.A. 107: 15397–15402. PubMed PMC
Los D.A., Zorina A., Sinetova M., Kryazhov S., Mironov K. and Zinchenko V.V. (2010) Stress sensors and signal transducers in cyanobacteria. Sensors 10: 2386–2415. PubMed PMC
Mahbub M., Hemm L., Yang Y., Kaur R., Carmen H., Engl C., et al. (2020) mRNA localization, reaction centre biogenesis and thylakoid membrane targeting in cyanobacteria. Nat. Plants 6: 1179–1191. PubMed
Malnoë A., Wang F., Girard-Bascou J., Wollman F.-A. and de Vitry C. (2014) Thylakoid FtsH protease contributes to photosystem II and cytochrome b(6)f remodeling in Chlamydomonas reinhardtii under stress conditions. Plant Cell 26: 373–390. PubMed PMC
Mann N.H., Novac N., Mullineaux C.W., Newman J., Bailey S. and Robinson C. (2000) Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp PCC 6803. FEBS Lett. 479: 72–77. PubMed
Maziak A., Heidorn-Czarna M., Weremczuk A. and Janska H. (2021) FTSH4 and OMA1 mitochondrial proteases reduce moderate heat stress-induced protein aggregation. Plant Physiol. 187: 769–786. PubMed PMC
McCleary W.R. (2017) Molecular mechanisms of phosphate homeostasis in Escherichia coli. In Escherichia Coli – Recent Advances on Physiology, Pathogenesis and Biotechnological Applications. Edited by Amidou, S. pp. 333–357. Intech Open, Rijeka.
Muramatsu M. and Hihara Y. (2003) Transcriptional regulation of genes encoding subunits of photosystem I during acclimation to high-light conditions in Synechocystis sp. PCC 6803. Planta 216: 446–453. PubMed
Nash D., Miyao M. and Murata N. (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim. Biophys. Acta 807: 127–133.
Nevo R., Charuvi D., Shimoni E., Schwarz R., Kaplan A., Ohad I., et al. (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO J. 26: 1467–1473. PubMed PMC
Nixon P.J., Michoux F., Yu J., Boehm M. and Komenda J. (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106: 1–16. PubMed PMC
Ogura T., Inoue K., Tatsuta T., Suzaki T., Karata K., Young K., et al. (1999) Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli. Mol. Microbiol. 31: 833–844. PubMed
Osanai T. and Tanaka K. (2007) Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. Plant Cell Physiol. 48: 908–914. PubMed
Qiao Z., Yokoyama T., Yan X.F., Beh I.T., Shi J., Basak S., et al. (2022) Cryo-EM structure of the entire FtsH-HflKC AAA protease complex. Cell Rep. 39: 110890. PubMed
Rachedi R., Foglino M. and Latifi A. (2020) Stress signaling in cyanobacteria: a mechanistic overview. Life 10: 312. PubMed PMC
Rast A., Schaffer M., Albert S., Wan W., Pfeffer S., Beck F., et al. (2019) Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane. Nat. Plants 5: 436–446. PubMed
Riediger M., Hernández-Prieto M.A., Song K., Hess W.R. and Futschik M.E. (2021) Genome-wide identification and characterization of Fur-binding sites in the cyanobacteria Synechocystis sp. PCC 6803 and PCC 6714. DNA Res 28: dsab023. PubMed PMC
Riediger M., Kadowaki T., Nagayama R., Georg J., Hihara Y. and Hess W.R. (2019) Biocomputational analyses and experimental validation identify the regulon controlled by the redox-responsive transcription factor RpaB. iScience 15: 316–331. PubMed PMC
Sacharz J., Bryan S.J., Yu J., Burroughs N.J., Spence E.M., Nixon P.J., et al. (2015) Sub-cellular location of FtsH proteases in the cyanobacterium Synechocystis sp PCC 6803 suggests localised PSII repair zones in the thylakoid membranes. Mol. Microbiol. 96: 448–462. PubMed PMC
Sakamoto W. (2003) Coordinated regulation of chloroplastic FTSH metalloproteases VAR1 and VAR2 in Arabidopsis. Gen. Genet. Syst. 78: 470.
Santos-Beneit F. (2015) The Pho regulon: a huge regulatory network in bacteria. Front. Microbiol. 6: 402. PubMed PMC
Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337. PubMed
Shao S., Cardona T. and Nixon P.J. (2018) Early emergence of the FtsH proteases involved in photosystem II repair. Photosynthetica 56: 163–177.
Shen G., Balasubramanian R., Wang T., Wu Y., Hoffart L.M., Krebs C., et al. (2007) SufR coordinates two [4Fe-4S]2+, 1+ clusters and functions as a transcriptional repressor of the sufBCDS operon and an autoregulator of sufR in cyanobacteria. J. Biol. Chem. 282: 31909–31919. PubMed
Silva P., Thompson E., Bailey S., Kruse O., Mullineaux C.W., Robinson C., et al. (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15: 2152–2164. PubMed PMC
Spät P., Maček B. and Forchhammer K. (2015) Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation. Front. Microbiol. 6: 248. PubMed PMC
Stirnberg M., Fulda S., Huckauf J., Hagemann M., Kraemer R. and Marin K. (2007) A membrane-bound FtsH protease is involved in osmoregulation in Synechocystis sp PCC 6803: the compatible solute synthesizing enzyme GgpS is one of the targets for proteolysis. Mol. Microbiol. 63: 86–102. PubMed
Stroebel D., Choquet Y., Popot J.L. and Picot D. (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426: 413–418. PubMed
Su Z., Olman V. and Xu Y. (2007) Computational prediction of Pho regulons in cyanobacteria. BMC Genomics 8: 156. PubMed PMC
Tomoyasu T., Gamer J., Bukau B., Kanemori M., Mori H., Rutman A.J., et al. (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J. 14: 2551–2560. PubMed PMC
Uniacke J. and Zerges W. (2007) Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 19: 3640–3654. PubMed PMC
Vavilin D., Yao D. and Vermaas W. (2007) Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803: kinetic analysis of pigment labeling with 15N and 13C. J. Biol. Chem. 282: 37660–37668. PubMed
Weixlbaumer A., Grünberger F., Werner F. and Grohmann D. (2021) Coupling of transcription and translation in Archaea: cues from the bacterial world. Front. Microbiol. 12: 661827. PubMed PMC
Wilde A. and Hihara Y. (2016) Transcriptional and posttranscriptional regulation of cyanobacterial photosynthesis. Biochim. Biophys. Acta 1857: 296–308. PubMed
Wiśniewski J.R. and Rakus D. (2014) Multi-enzyme digestion FASP and the ‘Total Protein Approach’-based absolute quantification of the Escherichia coli proteome. J. Proteom. 109: 322–331. PubMed
Yamamoto Y., Aminaka R., Yoshioka M., Khatoon M., Komayama K., Takenaka D., et al. (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth. Res. 98: 589–608. PubMed
Yeo W.S., Anokwute C., Marcadis P., Levitan M., Ahmed M., Bae Y., et al. (2020) A membrane-bound transcription factor is proteolytically regulated by the AAA+ protease FtsH in Staphylococcus aureus. J. Bacteriol. 202: e00019–20. PubMed PMC
Zhang P., Sicora C.I., Vorontsova N., Allahverdiyeva Y., Battchikova N., Nixon P.J., et al. (2007) FtsH protease is required for induction of inorganic carbon acquisition complexes in Synechocystis sp. PCC 6803. Mol. Microbiol. 65: 728–740. PubMed