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Evidence from the structure and function of cytochromes c2 that nonsulfur purple bacterial photosynthesis followed the evolution of oxygen respiration

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Abstract

Cytochromes c2 are the nearest bacterial homologs of mitochondrial cytochrome c. The sequences of the known cytochromes c2 can be placed in two subfamilies based upon insertions and deletions, one subfamily is most like mitochondrial cytochrome c (the small C2s, without significant insertions and deletions), and the other, designated large C2, shares 3- and 8-residue insertions as well as a single-residue deletion. C2s generally function between cytochrome bc1 and cytochrome oxidase in respiration (ca 80 examples known to date) and between cytochrome bc1 and the reaction center in nonsulfur purple bacterial photosynthesis (ca 21 examples). However, members of the large C2 subfamily are almost always involved in photosynthesis (12 of 14 examples). In addition, the gene for the large C2 (cycA) is associated with those for the photosynthetic reaction center (pufBALM). We hypothesize that the insertions in the large C2s, which were already functioning in photosynthesis, allowed them to replace the membrane-bound tetraheme cytochrome, PufC, that otherwise mediates between the small C2 or other redox proteins and photosynthetic reaction centers. Based upon our analysis, we propose that the involvement of C2 in nonsulfur purple bacterial photosynthesis was a metabolic feature subsequent to the evolution of oxygen respiration.

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References

  • Ambler RP, Wynn M (1973) The amino acid sequences of cytochromes c-551 from three species of Pseudomonas. Biochem J 131:485–498

    CAS  PubMed  Google Scholar 

  • Ambler RP, Daniel M, Hermoso J, Meyer TE, Bartsch RG, Kamen MD (1979) Cytochrome c2 sequence variation among the recognised species of purple nonsulphur photosynthetic bacteria. Nature 278:659–660

    Article  CAS  PubMed  Google Scholar 

  • Ambler RP, Meyer TE, Cusanovich MA, Kamen MD (1987) The amino acid sequence of the cytochrome c2 from the phototrophic bacterium Rhodopseudomonas globiformis. Biochem J 246:115–120

    CAS  PubMed  Google Scholar 

  • Ambler RP, Daniel M, Meyer TE, Kamen MD (1994) Amino acid sequences of cytochromes c2 and c′ from the moderately halophilic purple phototrophic bacterium Rhodospirillum salexigens. Biochimie 76:583–591

    Article  CAS  PubMed  Google Scholar 

  • Ambler RP, Meyer TE, Bartsch RG, Cusanovich MA (2001) An alternative to the accepted phylogeny of purple bacteria based on 16S rRNA: Analyses of the amino acid sequences of cytochromes c2 and c556 from Rhodobacter (Rhodovulum) sulfidophilus. Arch Biochem Biophys 388:25–33

    Article  CAS  PubMed  Google Scholar 

  • Axelrod HL, Okamura MY (2005) The structure and function of the cytochrome c2: reaction center electron transfer complex from Rhodobacter sphaeroides. Photosynth Res 85:101–114

    Article  CAS  PubMed  Google Scholar 

  • Axelrod HL, Feher G, Allen JP, Chirino AJ, Day MW, Hsu BT, Rees DC (1994) Crystallization and X-ray structure determination of cytochrome c2 from Rhodobacter sphaeroides in three crystal forms. Acta Crystallogr D 50:596–602

    Article  CAS  PubMed  Google Scholar 

  • Barber RD, Rott MA, Donohue TJ (1996) Characterization of a glutathione dependent formaldehyde dehydrogenase from Rhodobacter sphaeroides. J Bacteriol 178:1386–1393

    CAS  PubMed  Google Scholar 

  • Benning MM, Wesenberg G, Caffrey MS, Bartsch RG, Meyer TE, Cusanovich MA, Rayment I, Holden HM (1991) Molecular structure of cytochrome c2 isolated from Rhodobacter capsulatus determined at 2.5 Å resolution. J Mol Biol 220:673–685

    Article  CAS  PubMed  Google Scholar 

  • Benning MM, Meyer TE, Holden HM (1994) X-ray structure of the cytochrome c2 isolated from Paracoccus denitrificans at 1.7-Å resolution. Arch Biochem Biophys 310:460–466

    Article  CAS  PubMed  Google Scholar 

  • Bott M, Ritz D, Hennecke H (1991) The Bradyrhizobium japonicum cycM gene encodes a membrane-anchored homolog of mitochondrial cytochrome c. J Bacteriol 173:6766–6772

    CAS  PubMed  Google Scholar 

  • Camara-Artigas A, Williams JC, Allen JP (2001) Structure of cytochrome c2 from Rhodospirillum centenum. Acta Crystallogr D57:1498–1505

    CAS  Google Scholar 

  • Chan SK, Hsing M, Hormozdiari F, Cherkasov A (2007) Relationship between insertion/deletion (indel) frequency of proteins and essentiality. BMC Bioinformatics 8:227

    Article  PubMed  Google Scholar 

  • Daldal F, Cheng S, Applebaum J, Davidson E, Prince RC (1986) Cytochrome c2 is not essential for photosynthetic growth of Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A 83:2012–2016

    Article  CAS  PubMed  Google Scholar 

  • Donohue TJ, McEwan AG, Kaplan S (1986) Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides cytochrome c2 gene. J Bacteriol 168:962–972

    CAS  PubMed  Google Scholar 

  • Donohue TJ, McEwan AG, Van Doren S, Crofts AR, Kaplan S (1988) Phenotypic and genetic characterization of cytochrome c2 deficient mutants of Rhodobacter sphaeroides. Biochem 27:1918–1925

    Article  CAS  Google Scholar 

  • Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746

    Article  CAS  PubMed  Google Scholar 

  • Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microb Physiol 39:235–289

    Article  CAS  PubMed  Google Scholar 

  • Geremia S, Garau G, Vaccari L, Sgarra R, Viezzoli MS, Calligaris M, Randaccio L (2002) Cleavage of the iron-methionine bond in c-type cytochrome: crystal structure of oxidized and reduced cytochrome c2 from Rhodopseudomonas palustris and its ammonia complex. Prot Sci 11:6–17

    Article  CAS  Google Scholar 

  • Jenney FE, Daldal F (1993) A novel membrane-associated c-type cytochrome, cyt cy, can mediate the photosynthetic growth of Rhodobacter capsulatus and Rhodobacter sphaeroides. EMBO J 12:1283–1292

    CAS  PubMed  Google Scholar 

  • Kimura Y, Alric J, Vermeglio A, Masuda S, Hagiwara Y, Matsuura K, Shimada K, Nagashima KVP (2007) A new membrane-bound cytochrome c works as an electron donor to the photosynthetic reaction center complex in the purple bacterium, Rhodovulum sulfidophilum. J Biol Chem 282:6463–6472

    Article  CAS  PubMed  Google Scholar 

  • Margoliash E, Fitch WM (1968) Evolutionary variability of cytochrome c primary structures. Ann N Y Acad Sci 151:359–381

    Article  CAS  PubMed  Google Scholar 

  • Masuda S, Tsukatani Y, Kimura Y, Nagashima KV, Matsuura K (2002) Mutational analyses of the photosynthetic reaction center-bound triheme cytochrome subunit and cytochrome c2 in the purple bacterium, Rhodovulum sulfidophilum. Biochem 41:11211–11217

    Article  CAS  Google Scholar 

  • Menin L, Schoepp B, Parot P, Vermeglio A (1997) Photoinduced cyclic electron transfer in Rhodocyclus tenuis cells: participation of HiPIP or cyt c8 depending on the ambient redox potential. Biochem. 36:12183–12188

    Article  CAS  Google Scholar 

  • Meyer TE, Bansal AK (2005) Stabilization against hyperthermal denaturation through increased CG content can explain the discrepancy between whole genome and 16S rRNA analyses. Biochem. 44:11458–11465

    Article  CAS  Google Scholar 

  • Meyer TE, Cusanovich MA, Kamen MD (1986) Evidence against use of bacterial amino acid sequence data for construction of all-inclusive phylogenetic trees. Proc Natl Acad Sci USA 83:217–220

    Article  CAS  PubMed  Google Scholar 

  • Myllykallio H, Zannoni D, Daldal F (1999) The membrane-attached electron carrier cytochrome cy from Rhodobacter sphaeroides is functional in respiratory but not in photosynthetic electron transfer. Proc Natl Acad Sci USA 96:4348–4353

    Article  CAS  PubMed  Google Scholar 

  • Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80:373–386

    Article  CAS  PubMed  Google Scholar 

  • Öztürk Y, Lee DW, Mandaci S, Osyczka A, Prince RC, Daldal F (2008) Soluble variants of Rhodobacter capsulatus membrane-anchored cytochrome cy are efficient photosynthetic electron carriers. J Biol Chem 283:13964–13972

    Article  PubMed  Google Scholar 

  • Pitcher RS, Cheesman MR, Watmough NJ (2002) Molecular and spectroscopic analysis of the cytochrome cbb3 oxidase from Pseudomonas stutzeri. J Biol Chem 277:31474–31483

    Article  CAS  PubMed  Google Scholar 

  • Rott MA, Witthuhn VC, Schilke BA, Soranno M, Ali A, Donohue JG (1993) Genetic evidence for the role of isocytochrome c2 in photosynthetic growth of Rhodobacter sphaeroides spd mutants. J. Bact. 175:358–366

    CAS  PubMed  Google Scholar 

  • Salemme FR, Freer ST, Xuong NH, Alden RA, Kraut J (1973) The structure of oxidized cytochrome c2 of Rhodospirillum rubrum. J.Biol. Chem. 248:3910–3921

    CAS  PubMed  Google Scholar 

  • Samyn B, Fitch J, Meyer TE, Cusanovich MA, Van Beeumen JJ (1998) Purification and primary structure analysis of two cytochrome c2 isozymes from the purple phototrophic bacterium Rhodospirillum centenum. Biochim Biophys Acta 1384:345–355

    CAS  PubMed  Google Scholar 

  • Suyama T, Shigematsu T, Suzuki T, Tokiwa Y, Kanagawa T, Nagashima KVP, Hanada S (2002) Photosynthetic apparatus in Roseateles depolymerans 61A is transcriptionally induced by carbon limitation. Appl Environ Microbiol 68:1665–1673

    Article  CAS  PubMed  Google Scholar 

  • Tsukatani Y, Matsuura K, Masuda S, Shimada K, Hiraishi A, Nagashima KVP (2004) Phylogenetic distribution of unusual triheme to tetraheme cytochrome subunit in the reaction center complex of purple photosynthetic bacteria. Photosynth Res 79:83–91

    Article  CAS  PubMed  Google Scholar 

  • Turba A, Jetzek M, Ludwig B (1995) Purification of Paracoccus denitrificans cytochrome c552 and sequence analysis of the gene. Eur J Biochem 231:259–265

    CAS  PubMed  Google Scholar 

  • Van Driessche G, Vandenberghe I, Devreese B, Samyn B, Meyer TE, Leigh R, Cusanovich MA, Bartsch RG, Fischer U, Van Beeumen JJ (2003) Amino acid sequences and distribution of High-Potential Iron-Sulfur Proteins that donate electrons to the photosynthetic reaction center in phototrophic proteobacteria. J Mol Evol 57:181–199

    Article  PubMed  Google Scholar 

  • Van Driessche G, Devreese B, Fitch JC, Meyer TE, Cusanovich MA, Van Beeumen JJ (2006) GHP, a new c-type green heme protein from Halochromatium salexigens and other proteobacteria. FEBS J 273:2801–2811

    Article  PubMed  Google Scholar 

  • Wilson SM, Gleisten MP, Donohue TJ (2008) Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides. Microbiology 154:296–305

    Article  CAS  PubMed  Google Scholar 

  • Witthuhn VC Jr, Gao J, Hong S, Halls S, Rott MA, Wraight CA, Crofts AR, Donohue TJ (1997) Reactions of isocytochrome c2 in the photosynthetic electron transfer chain of Rhodobacter sphaeroides. Biochemistry 36:903–911

    Article  PubMed  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    CAS  PubMed  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer C (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    Article  CAS  PubMed  Google Scholar 

  • Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by a grant from the National Institutes of Health (GM21277) and by a research grant from the Bijzonder Onderzoeksfonds of Ghent University (B/06840/01).

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Correspondence to Terry Meyer.

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Communicated by Timothy Donohue.

M. Cusanovich: deceased.

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Meyer, T., Van Driessche, G., Ambler, R. et al. Evidence from the structure and function of cytochromes c2 that nonsulfur purple bacterial photosynthesis followed the evolution of oxygen respiration. Arch Microbiol 192, 855–865 (2010). https://doi.org/10.1007/s00203-010-0608-2

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  • DOI: https://doi.org/10.1007/s00203-010-0608-2

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