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
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
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
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
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
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
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
Barber RD, Rott MA, Donohue TJ (1996) Characterization of a glutathione dependent formaldehyde dehydrogenase from Rhodobacter sphaeroides. J Bacteriol 178:1386–1393
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
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
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
Camara-Artigas A, Williams JC, Allen JP (2001) Structure of cytochrome c2 from Rhodospirillum centenum. Acta Crystallogr D57:1498–1505
Chan SK, Hsing M, Hormozdiari F, Cherkasov A (2007) Relationship between insertion/deletion (indel) frequency of proteins and essentiality. BMC Bioinformatics 8:227
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
Donohue TJ, McEwan AG, Kaplan S (1986) Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides cytochrome c2 gene. J Bacteriol 168:962–972
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
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
Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microb Physiol 39:235–289
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
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
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
Margoliash E, Fitch WM (1968) Evolutionary variability of cytochrome c primary structures. Ann N Y Acad Sci 151:359–381
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
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
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
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
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
Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80:373–386
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
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
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
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
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
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
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
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
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
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
Wilson SM, Gleisten MP, Donohue TJ (2008) Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides. Microbiology 154:296–305
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
Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271
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
Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer C (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730
Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724
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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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