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New perspectives on bacterial ferredoxin evolution

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Summary

Recent evidence indicates that a gene transposition event occurred during the evolution of the bacterial ferredoxins subsequent to the ancestral intrasequence gene duplication. In light of this new information, the relationships among the bacterial ferredoxins were reexamined and an evolutionary tree consistent with this new understanding was derived. The bacterial ferredoxins can be divided into several groups based on their sequence properties; these include the clostridial-type ferredoxins, theAzotobacter-type ferredoxins, and a group containing the ferredoxins from the anaerobic, green, and purple sulfur bacteria. Based on sequence comparison, it was concluded that the amino-terminal domain of theAzotobacter-type ferredoxins, which contains the novel 3Fe∶3S cluster binding site, is homologous with the carboxyl-terminal domain of the ferredoxins from the anaerobic photosynthetic bacteria.

A number of ferredoxin sequences do not fit into any of the groups described above. Based on sequence properties, these sequences can be separated into three groups: a group containingMethanosarcina barkeri ferredoxin andDesulfovibrio desulfuricans ferredoxin II, a group containingDesulfovibrio gigas ferredoxin andClostridium thermoaceticum ferredoxin, and a group containingDesulfovibrio africanus ferredoxin I andBacillus stearothermophilus ferredoxin. The last two groups differ from all of the other bacterial ferredoxins in that they bind only one Fe∶S cluster per polypeptide, whereas the others bind two. Sequence examination indicates that the second binding site has been either partially or completely lost from these ferredoxins.Methanosarcina barkeri ferredoxin andDesulfovibrio desulfuricans ferredoxin II are of interest because, of all the ferredoxins whose sequences are presently known, they show the strongest evidence of internal gene duplication. However, the derived evolutionary tree indicates that they diverged from theAzotobacter-type ferredoxins well after the ancestral internal gene duplication. This apparent discrepancy is explained by postulating a duplication of one halfchain sequence and a deletion of the other halfchain. TheClostridium thermoaceticum andBacillus stearothermophilus groups diverged from this line and subsequently lost one of the Fe∶S binding sites.

It has recently become apparent that gene duplication is ubiquitous among the ferredoxins. Several organisms are now known to have a variety of ferredoxins with widely divergent properties. Unfortunately, in only one case are the sequences of more than one ferredoxin from the same organism known. Thus, although the major features of the bacterial ferredoxin tree are now understood, a complete bacterial phylogeny cannot be inferred until more sequence information is available.

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References

  • Adman ET, Sieker LC, Jensen LH (1976) Structure ofPeptococcus aerogenes ferredoxin: refinement at 2 Å resolution. J Biol Chem 251:3801–3806

    PubMed  Google Scholar 

  • Bell SH, Dickson DPE, Johnson CE, Cammack R, Hall DO, Rao KK (1982) Mossbauer spectroscopic evidence for the conversion of [4Fe−4S] clusters inBacillus stearothermophilus ferredoxin into [3Fe−3S] clusters. FEBS Lett 142:143–146

    PubMed  Google Scholar 

  • Benson MA, Mower HF, Yasunobu KT (1966) The amino acid sequence ofClostridium butyricum ferredoxin. Proc Natl Acad Sci USA 55:1532–1535

    PubMed  Google Scholar 

  • Bruschi M (1979) Amino acid sequence ofDesulfovibrio gigas ferredoxin: revisions. Biochem Biophys Res Commun 91: 623–628

    PubMed  Google Scholar 

  • Bruschi M, Hatchikian EC (1982) Non-heme iron proteins ofDesulfovibrio: the primary structure of ferredoxin I fromDesulfovibrio africanus. Biochimie 64:503–507

    PubMed  Google Scholar 

  • Bruschi M, Hatchikian EC, Le Gall J, Moura JJG, Xavier AV (1976) Purification, characterization and biological activity of three forms of ferredoxin from the sulfate-reducing bacteriumDesulfovibrio gigas. Biochim Biophys Acta 449:275–284

    PubMed  Google Scholar 

  • Buchanan BB, Arnon DI (1970) Ferredoxins: chemistry and function in photosynthesis, nitrogen fixation, and fermentative metabolism. Adv Enzymol 33:119–176

    PubMed  Google Scholar 

  • Cammack R, Rao KK, Hall DO, Moura JJG, Xavier AV, Bruschi M, Le Gall J, Deville A, Gayda JP (1977) Spectroscopic studies of the oxidation-reduction properties of three forms of ferredoxin fromDesulfovibrio gigas. Biochim Biophys Acta 490:311–321

    PubMed  Google Scholar 

  • Carter CW Jr, Kraut J, Freer ST, Alden RA (1974) Comparison of oxidation-reduction site geometries in oxidized and reducedChromatium high potential iron protein and oxidizedPeptococcus aerogenes ferredoxin. J Biol Chem 249:6339–6346

    PubMed  Google Scholar 

  • Dayhoff MO (1983) Evolutionary connections of biological kingdoms based on protein and nucleic acid sequence evidence. Precambrian Res 20:299–318

    Google Scholar 

  • Dayhoff MO, Barker WC, Hunt LT (1983) Establishing homologies in protein sequences. Methods Enzymol 91:524–545

    PubMed  Google Scholar 

  • Eck RV, Dayhoff MO (1966) Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences. Science 152:363–366

    Google Scholar 

  • Elliott JI, Yang SS, Ljungdahl LG, Travis J, Reilly CF (1982) Complete amino acid sequence of the 4Fe−4S, thermostable ferredoxin fromClostridium thermoaceticum. Biochemistry 21:3294–3298

    PubMed  Google Scholar 

  • George DG, Hunt LT, Dayhoff MO (1983) Sequence evidence for the symbiotic origins of chloroplasts and mitochondria. In: Schwemmler W, Schenk HEA (eds) Endocytobiology, vol II. Walter de Gruyter and Co, Berlin New York, pp 845–861

    Google Scholar 

  • Ghosh D, O'Donnell S, Furey W Jr, Robbins AH, Stout CD (1982) Iron-sulfur clusters and protein structure ofAzotobacter ferredoxin at 2.0 Å resolution. J Mol Biol 158:73–109

    PubMed  Google Scholar 

  • Guerlesquin F, Bruschi M, Bovier-Lapierre G, Bonicel J, Couchoud P (1983) Primary structure of the two (4Fe−4S) clusters of ferredoxin fromDesulfovibrio desulfuricans (strain Norway 4). Biochimie 65:43–47

    PubMed  Google Scholar 

  • Hall DO, Cammack R, Rao KK (1973) Ferredoxin in the evolution of photosynthetic systems from anaerobic bacteria to higher plants. Space Life Sci 4:455–468

    PubMed  Google Scholar 

  • Hase T, Ohmiya N, Matsubara H, Mullinger RN, Rao KK, Hall DO (1976) Amino acid sequence of a four-iron-four-sulfur ferredoxin isolated fromBacillus stearothermophilus. Biochem J 159:55–63

    PubMed  Google Scholar 

  • Hase T, Matsubara H, Evans MCW (1977) Amino acid sequence ofChromatium vinosum ferredoxin: revisions. J Biochem (Tokyo) 81:1745–1749

    Google Scholar 

  • Hase T, Wakabayashi S, Matsubara H, Evans MCW, Jennings JV (1978a) Amino acid sequence of a ferredoxin fromChlorobium thiosulfatophilum strain Tassajara, a photosynthetic green sulfur bacterium. J Biochem (Tokyo) 83:1321–1325

    Google Scholar 

  • Hase T, Wakabayashi S, Matsubara H, Kerscher L, Oesterhelt D, Rao KK, Hall DO (1978b) Complete amino acid sequence ofHalobacterium halobium ferredoxin containing an N∈-acetyllysine residue. J Biochem (Tokyo) 83:1657–1670

    Google Scholar 

  • Hase T, Wakabayashi S, Matsubara H, Ohmori D, Suzuki K (1978c)Pseudomonas ovalis ferredoxin: similarity toAzotobacter andChromatium ferredoxins. FEBS Lett 91:315–319

    PubMed  Google Scholar 

  • Hase T, Wakabayashi S, Matsubara H, Imai T, Matsumoto T, Tobari J (1979)Mycobacterium smegmatis ferredoxin: a unique distribution of cysteine residues constructing ironsulfur clusters. FEBS Lett 103:224–228

    PubMed  Google Scholar 

  • Hase T, Wakabayashi S, Matsubara H, Mevarech M, Werber MM (1980) Amino acid sequence of 2Fe−2S ferredoxin from an extreme halophile,Halobacterium of the Dead Sea. Biochim Biophys Acta 623:139–145

    PubMed  Google Scholar 

  • Hausinger RP, Moura I, Moura JJG, Xavier AV, Santos MH, LeGall J, Howard JB (1982) Amino acid sequence of a 3Fe∶ 3S ferredoxin from the “archaebacterium”Methanosarcina barkeri (DSM 800). J Biol Chem 257:14192–14197

    PubMed  Google Scholar 

  • Hille R, Yoshida T, Tarr GE, Williams CH Jr, Ludwig ML, Fee JA, Kent TA, Huynh BH, Munck E (1983) Studies of the ferredoxin fromThermus thermophilus. J Biol Chem 258:13008–13013

    PubMed  Google Scholar 

  • Howard JB, Lorsbach TW, Ghosh D, Melis K, Stout CD (1983) Structure ofAzotobacter vinelandii 7Fe ferredoxin: amino acid sequence and electron density maps of residues. J Biol Chem 258:508–522

    PubMed  Google Scholar 

  • Hunt LT, George DG, Yeh LS, Dayhoff MO (1984) Evolution of prokaryote and eukaryote lines inferred from sequence evidence. Orig Life 14:657–664

    PubMed  Google Scholar 

  • Huynh BH, Moura JJG, Moura I, Kent TA, LeGall J, Xavier AV, Munck E (1980) Evidence for a three-iron center in a ferredoxin fromDesulfovibrio gigas: Mossbauer and EPR studies. J Biol Chem 255:3242–3244

    PubMed  Google Scholar 

  • Johnson MK, Spiro TG, Mortenson LE (1982) Resonance Raman and electron paramagnetic resonance studies on oxidized and ferricyanide-treatedClostridium pasteurianum ferredoxin: vibrational assignments from34S shifts and evidence for conversion of 4 to 3 iron-sulfur clusters via oxidative damage. J Biol Chem 257:2447–2452

    PubMed  Google Scholar 

  • Lovenberg W, Buchanan BB, Rabinowitz JC (1963) Studies on the chemical nature of clostridial ferredoxin. J Biol Chem 238:3899–3913

    PubMed  Google Scholar 

  • Matsubara H, Hase T, Wakabayashi S, Wada K (1980) Structure and evolution of chloroplast- and bacterial-type ferredoxins. In: Sigman DS, Brazier MAB (eds) The evolution of protein structure and function. Academic Press, New York London, pp 245–266

    Google Scholar 

  • Matsubara H, Inoue K, Hase T, Hiura H, Kakuno T, Yamashita J, Horio T (1983) Structure of the extracellular ferredoxin fromRhodospirillum rubrum: close similarity to clostridial ferredoxins. J Biochem (Tokyo) 93:1385–1390

    Google Scholar 

  • Orme-Johnson WH (1973) Tryptic cleavage ofClostridium acidi-urici apoferredoxin, and reconstitution of the separated fragments. Biochem Soc Trans 1:30–31

    Google Scholar 

  • Rall SC, Bolinger RE, Cole RD (1969) The amino acid sequence of ferredoxin fromClostridium acidi-urici. Biochemistry 8:2486–2496

    PubMed  Google Scholar 

  • Sato S, Nakazawa K, Hon-Nami K, Oshima T (1981) Purification, some properties and amino acid sequence ofThermus thermophilus HB8 ferredoxin. Biochim Biophys Acta 668:277–289

    PubMed  Google Scholar 

  • Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science 199:395–403

    PubMed  Google Scholar 

  • Tanaka M, Nakashima T, Benson A, Mower H, Yasunobu KT (1966) The amino acid sequence ofClostridium pasteurianum ferredoxin. Biochemistry 5:1666–1681

    PubMed  Google Scholar 

  • Tanaka M, Haniu M, Matsueda G, Yasunobu KT, Himes RH, Akagi JM, Barnes EM, Devanathan T (1971) The primary structure of theClostridium tartarivorum ferredoxin, a heat-stable ferredoxin. J Biol Chem 246:3953–3960

    PubMed  Google Scholar 

  • Tanaka M, Haniu M, Yasunobu KT, Himes RH, Akagi JM (1973) The primary structure of theClostridium thermosaccharolyticum ferredoxin, a heat-stable ferredoxin. J Biol Chem 248:5215–5217

    PubMed  Google Scholar 

  • Tanaka M, Haniu M, Yasunobu KT, Evans MCW, Rao KK (1974a) Amino acid sequence of ferredoxin from a photosynthetic green bacterium,Chlorobium limicola. Biochemistry 13:2953–2959

    PubMed  Google Scholar 

  • Tanaka M, Haniu M, Yasunobu KT, Jones JB, Stadtman TC (1974b) Amino acid sequence determination of theClostridium M-E ferredoxin and a comment on the role of the aromatic residues in the clostridial ferredoxins. Biochemistry 13:5284–5289

    PubMed  Google Scholar 

  • Tanaka M, Haniu M, Yasunobu KT, Evans MCW, Rao KK (1975) The amino acid sequence of ferredoxin II fromChlorobium limicola, a photosynthetic green bacterium. Biochemistry 14:1938–1943

    PubMed  Google Scholar 

  • Thomson AJ, Robinson AE, Johnson MK, Moura JJG, Moura I, Xavier AV, LeGall J (1981) The three-iron cluster in a ferredoxin fromDesulfovibrio gigas: a low-temperature magnetic circular dichroism study. Biochim Biophys Acta 670:93–100

    PubMed  Google Scholar 

  • Tsukihara T, Homma K, Fukuyama K, Katsube Y, Hase T, Matsubara H, Tanaka N, Kakudo M (1981) Preliminary x-ray diffraction studies on a [4Fe−4S] ferredoxin fromBacillus thermoproteolyticus. J Mol Biol 152:821–823

    PubMed  Google Scholar 

  • Tsukihara Y, Katsube Y, Hase T, Wada K, Matsubara H (1982) Evolutionary relationship between [2Fe−2S] ferredoxins and an ancestral ferredoxin. In: Kimura M (ed) Molecular evolution, protein polymorphism and the neutral theory. Japan Scientific Societies Press, Tokyo, and Springer-Verlag, Berlin, pp 299–312

    Google Scholar 

  • Tsunoda JN, Yasunobu KT, Whiteley HR (1968) Non-heme iron proteins: IX. The amino acid sequence of ferredoxin fromMicrococcus aerogenes. J Biol Chem 243:6262–6272

    PubMed  Google Scholar 

  • Yasunobu KT, Tanaka M (1973a) The types, distribution in nature, structure-function, and evolutionary data of the ironsulfur proteins. In: Lovenberg W (ed) Iron-sulfur proteins, vol II. Academic Press, New York London, pp 27–130

    Google Scholar 

  • Yasunobu KT, Tanaka M (1973b) The evolution of iron-sulfur protein containing organisms. Syst Zool 22:570–589

    Google Scholar 

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George, D.G., Hunt, L.T., Yeh, LS.L. et al. New perspectives on bacterial ferredoxin evolution. J Mol Evol 22, 20–31 (1985). https://doi.org/10.1007/BF02105801

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