Advertisement

Photosynthetica

, Volume 56, Issue 1, pp 163–177 | Cite as

Early emergence of the FtsH proteases involved in photosystem II repair

  • S. Shao
  • T. Cardona
  • P. J. Nixon
Open Access
Article

Abstract

Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

Additional key words

AAA+ protease chloroplast cyanobacteria evolution photoprotection water oxidation 

Abbreviations

AAA+

ATPase associated with diverse activities

CPR

candidate phyla radiation

HGT

horizontal gene transfer

RC

reaction center

ROS

reactive oxygen species

Supplementary material

11099_2018_769_MOESM1_ESM.pdf (70 kb)
Supplementary material, approximately 70.4 KB.

References

  1. Arlt H., Tauer R., Feldmann H. et al.: The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria.–Cell 85: 875–885, 1996.PubMedCrossRefGoogle Scholar
  2. Bailey S., Silva P., Nixon P. et al.: Auxiliary functions in photosynthesis: the role of the FtsH protease.–Biochem. Soc. Trans. 29: 455–459, 2001.PubMedCrossRefGoogle Scholar
  3. Bailey S., Thompson E., Nixon P.J. et al: A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo.–J. Biol. Chem. 277: 2006–2011, 2002.PubMedCrossRefGoogle Scholar
  4. Baker M.J., Tatsuta T., Langer T.: Quality control of mitochondrial proteostasis.–CSH Perspect. Biol. 3: 1–19, 2011.Google Scholar
  5. Battistuzzi F.U., Hedges S.B.: A major clade of prokaryotes with ancient adaptations to life on land.–Mol. Biol. Evol. 26: 335–343, 2009.PubMedCrossRefGoogle Scholar
  6. Beanland T.J.: Evolutionary relationships between “Q-type” photosynthetic reaction centres: Hypothesis-testing using parsimony.–J. Theor. Biol. 145: 535–545, 1990.PubMedCrossRefGoogle Scholar
  7. Becková M., Yu J., Krynická V. et al.: Structure of Psb29/Thf1 and its association with the FtsH protease complex involved in photosystem II repair in cyanobacteria.–Philos. T. R. Soc. B 372:1730, 2017.CrossRefGoogle Scholar
  8. Bengtson S., Sallstedt T., Belivanova V. et al.: Threedimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae.–PLoS Biol. 15: e2000735, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bhaya D., Grossman A.R., Steunou A.-S. et al.: Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses.–ISME J. 1: 703–713, 2007.PubMedCrossRefGoogle Scholar
  10. Bieniossek C., Niederhauser B., Baumann U.M.: The crystal structure of apo-FtsH reveals domain movements necessary for substrate unfolding and translocation.–P. Natl. Acad. Sci. USA 106: 21579–21584, 2009.CrossRefGoogle Scholar
  11. Bieniossek C., Schalch T., Bumann M. et al.: The molecular architecture of the metalloprotease FtsH.–P. Natl. Acad. Sci. USA 103: 3066–3071, 2006.CrossRefGoogle Scholar
  12. Bittner L.M., Arends J., Narberhaus F.: When, how and why? Regulated proteolysis by the essential FtsH protease in Escherichia coli.–Biol. Chem. 398: 625–635, 2017.PubMedCrossRefGoogle Scholar
  13. Boehm M., Yu J., Krynicka V. et al.: Subunit organization of a Synechocystis hetero-oligomeric thylakoid FtsH complex involved in Photosystem II repair.–Plant Cell 24: 3669–3683, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bombar D., Heller P., Sanchez-Baracaldo P. et al.: Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria.–ISME J. 8: 2530–2542, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brocks J.J., Love G.D., Summons R.E. et al.: Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea.–Nature 437: 866–870, 2005.PubMedCrossRefGoogle Scholar
  16. Bryant D.A., Costas A.M.G., Maresca J.A. et al.: Candidatus Chloracidobacterium thermophilum: An aerobic phototrophic acidobacterium.–Science 317: 523–526, 2007.PubMedCrossRefGoogle Scholar
  17. Bryant D.A., Liu Z., Li T. et al.: Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, Acidobacteria.–In: Burnap R.L., Vermaas W. (ed.): Functional Genomics and Evolution of Photosynthetic Systems. Pp. 47–102. Springer, Dordrecht 2012.CrossRefGoogle Scholar
  18. Butterfield N.J.: Early evolution of the Eukaryota.–Palaeontology 58: 5–17, 2015.CrossRefGoogle Scholar
  19. Capella-Gutiérrez S., Silla-Martínez J.M., Gabaldón T.: trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses.–Bioinformatics 25: 1972–1973, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cardona T.: A fresh look at the evolution and diversification of photochemical reaction centers.–Photosynth. Res. 126: 111–134, 2015.PubMedCrossRefGoogle Scholar
  21. Cardona T.: Origin of bacteriochlorophyll a and the early diversification of photosynthesis.–PLoS ONE 11: e0151250, 2016a.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cardona T.: Photosystem II is a chimera of reaction centers.–J. Mol. Evol. 84: 149–151, 2017.PubMedCrossRefGoogle Scholar
  23. Cardona T.: Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?–Front. Plant Sci. 7: 257, 2016b.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cardona T., Sánchez-Baracaldo P., Rutherford A.W. et al.: Molecular evidence for the early evolution of photosynthetic water oxidation.–bioRxiv: https://doi.org/10.1101/109447, 2017.Google Scholar
  25. Chen J., Burke J.J., Velten J. et al.: FtsH11 protease plays a critical role in Arabidopsis thermotolerance.–Plant J. 48: 73–84, 2006.PubMedCrossRefGoogle Scholar
  26. Cheregi O., Sicora C., Kós P.B. et al.: The role of the FtsH and Deg proteases in the repair of UV-B radiation-damaged Photosystem II in the cyanobacterium Synechocystis PCC 6803.–BBA-Bioenergetics 1767: 820–828, 2007.PubMedCrossRefGoogle Scholar
  27. Ciccarelli F.D., Doerks T., von Mering C. et al.: Toward automatic reconstruction of a highly resolved tree of life.–Science 311: 1283–1287, 2006.PubMedCrossRefGoogle Scholar
  28. Cole J.K., Hutchison J.R., Renslow R.S. et al.: Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotrophheterotroph interactions.–Front. Microbiol. 5: 109, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Crowe S.A., Jones C., Katsev S. et al.: Photoferrotrophs thrive in an Archean Ocean analogue.–P. Natl. Acad. Sci. USA 105: 15938–15943, 2008.CrossRefGoogle Scholar
  30. Dagan T., Roettger M., Stucken K. et al.: Genomes of stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids.–Genome Biol. Evol. 5: 31–44, 2013.PubMedCrossRefGoogle Scholar
  31. David L.A., Alm E.J.: Rapid evolutionary innovation during an Archaean genetic expansion.–Nature 469: 93–96, 2011.PubMedCrossRefGoogle Scholar
  32. Dutilh B.E., Snel B., Ettema T.J.G. et al.: Signature genes as a phylogenomic tool.–Mol. Biol. Evol. 25: 1659–1667, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dvořák P., Casamatta D.A., Poulíčková A. et al.: Synechococcus: 3 billion years of global dominance.–Mol. Ecol. 23: 5538–5551, 2014.PubMedCrossRefGoogle Scholar
  34. Dvořák P., Hindák F., Hašler P. et al.: Morphological and molecular studies of Neosynechococcus sphagnicola, gen. et sp. nov. (Cyanobacteria, Chroococcales).–Phytotaxa 170: 24–34, 2011.CrossRefGoogle Scholar
  35. Eddy S.R.: Accelerated profile HMM searches.–PLoS Comput. Biol. 7: e1002195, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ferro M., Brugière S., Salvi D. et al.: AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins.–Mol. Cell. Proteomics 9: 1063–1084, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Finn R.D., Coggill P., Eberhardt R.Y. et al.: The Pfam protein families database: towards a more sustainable future.–Nucleic Acids Res. 44: D279–D285, 2016.PubMedCrossRefGoogle Scholar
  38. Fischer W.W., Hemp J., Johnson J.E.: Evolution of oxygenic photosynthesis.–Annu. Rev. Earth Pl. Sc. 44: 647–683, 2016.CrossRefGoogle Scholar
  39. Frickey T., Lupas A.N.: Phylogenetic analysis of AAA proteins.–J. Struct. Biol. 146: 2–10, 2004.PubMedCrossRefGoogle Scholar
  40. Greening C., Carere C.R., Rushton-Green R. et al.: Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging.–P. Natl. Acad. Sci. USA 112: 10497–10502, 2015.CrossRefGoogle Scholar
  41. Guindon S., Dufayard J.F., Lefort V. et al.: New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0.–Syst. Biol. 59: 307–321, 2010.PubMedCrossRefGoogle Scholar
  42. Gupta R.S., Lorenzini E.: Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the Bacteroidetes and Chlorobi species.–BMC Evol. Biol. 7: 71, 2007.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Harel A., Karkar S., Cheng S. et al.: Deciphering primordial cyanobacterial genome functions from protein network analysis.–Curr. Biol. 25: 628–634, 2015.PubMedCrossRefGoogle Scholar
  44. Heazlewood J.L., Tonti-Filippini J.S., Gout A.M. et al.: Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, indicates plantspecific mitochondrial proteins.–Plant Cell 16: 241–256, 2004.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hilton J.A., Foster R.A., Tripp H.J. et al.: Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont.–Nat. Commun. 4: 1767, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hohmann-Marriott M.F., Blankenship R.E.: Evolution of photosynthesis.–Annu. Rev. Plant Biol. 62: 515–548, 2011.PubMedCrossRefGoogle Scholar
  47. Hug L.A., Baker B.J., Anantharaman K. et al: A new view of the tree of life.–Nat. Microbiol. 1: 16048, 2016.PubMedCrossRefGoogle Scholar
  48. Iyer L.M., Leipe D.D., Koonin E. V. et al.: Evolutionary history and higher order classification of AAA+ ATPases.–J. Struct. Biol. 146: 11–31, 2004.PubMedCrossRefGoogle Scholar
  49. Jun S.-R., Sims G.E., Wu G.A. et al.: Whole-proteome phylogeny of prokaryotes by feature frequency profiles: An alignment-free method with optimal feature resolution.–P. Natl. Acad. Sci. USA 107: 133–138, 2010.CrossRefGoogle Scholar
  50. Kadirjan-Kalbach D.K., Yoder D.W., Ruckle M.E. et al.: FtsHi1/ARC1 is an essential gene in Arabidopsis that links chloroplast biogenesis and division.–Plant J. 72: 856–867, 2012.PubMedCrossRefGoogle Scholar
  51. Kato Y., Sakamoto W.: Protein quality control in chloroplasts: A current model of D1 protein degradation in the photosystem II repair cycle.–J. Biochem. 146: 463–469, 2009.PubMedCrossRefGoogle Scholar
  52. Kirstein J., Molière N., Dougan D.A. et al.: Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases.–Nat. Rev. Microbiol. 7: 589–599, 2009.PubMedCrossRefGoogle Scholar
  53. Komárek J., Kaštovský J., Mareš J. et al.: Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach.–Preslia 86: 295–335, 2014.Google Scholar
  54. Komenda J., Barker M., Kuviková S. et al.: 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, 2006.PubMedCrossRefGoogle Scholar
  55. Komenda J., Hassan H.A.G., Diner B.A. et al.: Degradation of the photosystem II D1 and D2 proteins in different strains of the cyanobacterium Synechocytis PCC 6803 varying with respect to the type and level of psbA transcript.–Plant Mol. Biol. 42: 635–645, 2000.PubMedCrossRefGoogle Scholar
  56. Komenda J., Knoppová J., Krynická V. et al.: 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.–BBA-Bioenergetics 1797: 566–575, 2010.PubMedCrossRefGoogle Scholar
  57. Komenda J., Sobotka R., Nixon P.J.: Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria.–Curr. Opin. Plant Biol. 15: 245–251, 2012.PubMedCrossRefGoogle Scholar
  58. Komenda J., Tichý M., Prášil O. et al.: 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, 2007.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Krynická V., Shao S., Nixon P.J. et al.: Accessibility controls selective degradation of photosystem II subunits by FtsH protease.–Nat. Plants 1: 15168, 2015.PubMedCrossRefGoogle Scholar
  60. Krynická V., Tichý M., Krafl J. et al.: 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, 2014.PubMedCrossRefGoogle Scholar
  61. Lee S., Augustin S., Tatsuta T. et al.: Electron cryomicroscopy structure of a membrane-anchored mitochondrial AAA protease.–J. Biol. Chem. 286: 4404–4411, 2011.PubMedCrossRefGoogle Scholar
  62. Leonhard K., Herrmann J.M., Stuart R.A. et al: AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria.–EMBO J. 15: 4218–4229, 1996.PubMedPubMedCentralGoogle Scholar
  63. Letunic I., Bork P.: Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees.–Nucleic Acids Res. 44: W242–W245, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Lu X., Zhang D., Li S. et al.: FtsHi4 is essential for embryogenesis due to its influence on chloroplast development in Arabidopsis.–PLoS ONE 9: e99741, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lyons T.W., Reinhard C.T., Planavsky N.J.: The rise of oxygen in Earth’s early ocean and atmosphere.–Nature 506: 307–315, 2014.PubMedCrossRefGoogle Scholar
  66. Mann N.H., Novac N., Mullineaux C.W. et al.: Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803.–FEBS Lett. 479: 72–77, 2000.PubMedCrossRefGoogle Scholar
  67. Marin J., Battistuzzi F.U., Brown A.C. et al.: The timetree of prokaryotes: new insights into their evolution and speciation.–Mol. Biol. Evol. 34: 437–446, 2017.PubMedGoogle Scholar
  68. Mistry J., Finn R.D., Eddy S.R. et al.: Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions.–Nucleic Acids Res. 41: e121, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mix L.J., Haig D., Cavanaugh C.M.: Phylogenetic analyses of the core antenna domain: Investigating the origin of photosystem I.–J. Mol. Evol. 60: 153–163, 2005.PubMedCrossRefGoogle Scholar
  70. Mulkidjanian A.Y., Koonin E. V., Makarova K.S. et al.: The cyanobacterial genome core and the origin of photosynthesis.–P. Natl. Acad. Sci. USA 103: 13126–13131, 2006.CrossRefGoogle Scholar
  71. Nei M., Gu X., Sitnikova T.: Evolution by the birth-and-death process in multigene families of the vertebrate immune system.–P. Natl. Acad. Sci. USA 94: 7799–7806, 1997.CrossRefGoogle Scholar
  72. Nei M., Rooney A.P.: Concerted and birth-and-death evolution of multigene families.–Annu. Rev. Genet. 39: 121–152, 2005.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Nishimura K., Kato Y., Sakamoto W.: Chloroplast proteases: updates on proteolysis within and across suborganellar compartments.–Plant Physiol. 171: 2280–2293, 2016.PubMedPubMedCentralGoogle Scholar
  74. Nitschke W., William Rutherford A.: Photosynthetic reaction centres: variations on a common structural theme?–Trends Biochem. Sci. 16: 241–245, 1991.PubMedCrossRefGoogle Scholar
  75. Piechota J., Kolodziejczak M., Juszczak I. et al.: Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana.–J. Biol. Chem. 285: 12512–12521, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pittis A.A., Gabaldón T.: Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry.–Nature 531: 101–104, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ponce-Toledo R.I., Deschamps P., López-García P. et al.: An early-branching freshwater cyanobacterium at the origin of plastids.–Curr. Biol. 27: 386–391, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Quaiser A., Ochsenreiter T., Lanz C. et al.: Acidobacteria form a coherent but highly diverse group within the bacterial domain: Evidence from environmental genomics.–Mol. Microbiol. 50: 563–575, 2003.PubMedCrossRefGoogle Scholar
  79. Rainey R.N., Glavin J.D., Chen H.-W. et al: A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space.–Mol. Cell. Biol. 26: 8488–8497, 2006.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Rexroth S., Mullineaux C.W., Ellinger D. et al.: The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains.–Plant Cell 23: 2379–2390, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Rinke C., Schwientek P., Sczyrba A. et al.: Insights into the phylogeny and coding potential of microbial dark matter.–Nature 499: 431–437, 2013.PubMedCrossRefGoogle Scholar
  82. Sacharz J., Bryan S.J., Yu J. et al.: 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, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sakamoto W., Zaltsman A., Adam Z. et al.: Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes.–Plant Cell 15: 2843–2855, 2003.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Sedaghatmehr M., Mueller-Roeber B., Balazadeh S.: The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis.–Nat. Commun. 7: 12439, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Segata N., Börnigen D., Morgan X.C. et al.: PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes.–Nat. Commun. 4: 2304, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Smakowska E., Czarna M., Janska H.: Mitochondrial ATPdependent proteases in protection against accumulation of carbonylated proteins.–Mitochondrion 19: 245–251, 2014.PubMedCrossRefGoogle Scholar
  87. Shimodaira H., Hasegawa M.: Multiple comparisons of loglikelihoods with applications to phylogenetic inference.–Mol. Biol. Evol. 16: 1114–1116, 1999.CrossRefGoogle Scholar
  88. Silva P., Thompson E., Bailey S. et al.: FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803.–Plant Cell 15: 2152–2164, 2003.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Snider J., Thibault G., Houry W.A.: The AAA+ superfamily of functionally diverse proteins.–Genome Biol. 9: 216, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sousa F.L., Shavit-Grievink L., Allen J.F. et al.: Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis.–Genome Biol. Evol. 5: 200–216, 2013.PubMedCrossRefGoogle Scholar
  91. Steglich G., Neupert W., Langer T.: Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria.–Mol. Cell. Biol. 19: 3435–3442, 1999.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Stirnberg M., Fulda S., Huckauf J. et al.: Osmoregulation in Synechocystis sp. PCC 6803: the compatible solute synthesizing enzyme GgpS is one of the targets for proteolysis.–Mol. Microbiol. 63: 86–102, 2007.PubMedCrossRefGoogle Scholar
  93. Suno R., Niwa H., Tsuchiya D. et al.: Structure of the whole cytosolic region of ATP-dependent protease FtsH.–Mol. Cell 22: 575–585, 2006.PubMedCrossRefGoogle Scholar
  94. Suno R., Shimoyama M., Abe A. et al.: Conformational transition of the lid helix covering the protease active site is essential for the ATP-dependent protease activity of FtsH.–FEBS Lett.5 586: 3117–3121, 2012.PubMedCrossRefGoogle Scholar
  95. Takahashi S., Badger M.R.: Photoprotection in plants: A new light on photosystem II damage.–Trends Plant Sci. 16: 53–60, 2011.PubMedCrossRefGoogle Scholar
  96. Tice M.M., Lowe D.R.: Photosynthetic microbial mats in the 3,416-Myr-old ocean.–Nature 431: 549–552, 2004.PubMedCrossRefGoogle Scholar
  97. Tomoyasu T., Yamanaka K., Murata K. et al.: Topology and subcellular localization of FtsH protein in Escherichia coli.–J. Bacteriol. 175: 1352–1357, 1993.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Urantowka A., Knorpp C., Olczak T. et al.: Plant mitochondria contain at least two i-AAA-like complexes.–Plant Mol. Biol. 59: 239–252, 2005.PubMedCrossRefGoogle Scholar
  99. Vostrukhina M., Popov A., Brunstein E. et al.: The structure of Aquifex aeolicus FtsH in the ADP-bound state reveals a C2-symmetric hexamer.–Acta Crystallogr. D 71: 1307–1318, 2015.PubMedCrossRefGoogle Scholar
  100. Wagner R., Aigner H., Funk C.: FtsH proteases located in the plant chloroplast.–Physiol. Plantarum 145: 203–214, 2012.CrossRefGoogle Scholar
  101. Wagner R., Aigner H., Pružinská A. et al.: Fitness analyses of Arabidopsis thaliana mutants depleted of FtsH metalloproteases and characterization of three FtsH6 deletion mutants exposed to high light stress, senescence and chilling.–New Phytol. 191: 449–458, 2011.PubMedCrossRefGoogle Scholar
  102. Ward N.L., Challacombe J.F., Janssen P.H. et al.: Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils.–Appl. Environ. Microbiol. 75: 2046–2056, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Wu M., Eisen J.A.: A simple, fast, accurate method of phylogenomic inference.–Genome Biol. 9: R151, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yamada-Inagawa T., Okuno T., Karata K. et al.: Conserved pore residues in the AAA protease FtsH are important for proteolysis and its coupling to ATP hydrolysis.–J. Biol. Chem. 278: 50182–50187, 2003.PubMedCrossRefGoogle Scholar
  105. Yamada K.D., Tomii K., Katoh K.: Application of the MAFFT sequence alignment program to large data - Reexamination of the usefulness of chained guide trees.–Bioinformatics 32: 3246–3251, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Yu F.: Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes.–Plant Physiol. 138: 1957–1966, 2005.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Yu F., Park S., Rodermel S.R.: The Arabidopsis FtsH metalloprotease gene family: Interchangeability of subunits in chloroplast oligomeric complexes.–Plant J. 37: 864–876, 2004.PubMedCrossRefGoogle Scholar
  108. Zakon H.H.: Convergent evolution on the molecular level.–Brain. Behav. Evol. 59: 250–261, 2002.PubMedCrossRefGoogle Scholar
  109. Zaltsman A., Ori N., Adam Z.: Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis.–Plant Cell 17: 2782–2790, 2005.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zehr J.P., Bench S.R., Carter B.J. et al.: Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II.–Science 322: 1110–1112, 2008.PubMedCrossRefGoogle Scholar
  111. Zelisko A., García-Lorenzo M., Jackowski G. et al.: AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence.–P. Natl. Acad. Sci. USA 102: 13699–13704, 2005.CrossRefGoogle Scholar
  112. Zeng Y., Feng F., Medová H. et al.: Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes.–P. Natl. Acad. Sci. USA 111: 7795–7800, 2014.CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  1. 1.Department of Life Sciences, Sir Ernst Chain Building – Wolfson Laboratories, Imperial College LondonSouth Kensington CampusLondonUK

Personalised recommendations