Close Similarity to Functionally Unrelated Mitochondrial Cytochrome C (Photosynthetic Bacteria/Amino-Acid Sequence/Molecular Evolution) RICHARD P

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Close Similarity to Functionally Unrelated Mitochondrial Cytochrome C (Photosynthetic Bacteria/Amino-Acid Sequence/Molecular Evolution) RICHARD P Proc. Nat. Acad. Sci. USA Vol. 73, No. 2, pp. 472-475, February 1976 Biochemistry Primary structure determination of two cytochromes c2: Close similarity to functionally unrelated mitochondrial cytochrome c (photosynthetic bacteria/amino-acid sequence/molecular evolution) RICHARD P. AMBLER*, TERRANCE E. MEYERt, AND MARTIN D. KAMENt § * Department of Molecular Biology, University of Edinburgh, Edinburgh EH9 3JR, Scotland; tDepartment of Chemistry, University of California, San Diego, La Jolla, Calif. 92093; and *Chemical-Biological Development Laboratory, University of Southern Cai ornia, Los Angeles, Calif. 90007 Contributed by Martin D. Kamen, December 12,1975 ABSTRACT The amino-acid sequences of the cyto- We have been studying the amino-acid sequences of the chromes c2 from the photosynthetic non-sulfur purple bacte- Rhodospirillaceae cytochromes c2 and find that they can be ria Rhodomicrobium vannielii and- Rhiodopseudomonas viri- divided at present into at least two groups on the basis of the dis have been determined. Only a single residue deletion (at position 11 in horse cytochrome c) is necessary to align the number of insertions and deletions which must be postulated sequences with those of mitochondrial cytochromes c. The to align them with mitochondrial cytochrome c. One of overall sequence similarity between these cytochromes c2 these, which includes the proteins from Rps. palustris, Rps. and mitochondrial cytochromes c is closer than that between capsulata, Rps. spherotdes (R. P. Ambler, T. E. Meyer, R. G. mitochondrial cytochromes c and the other cytochromes c2 Bartsch, and M. D. Kamen, unpublished results, see ref. 13), of known sequence, and in the latter multiple insertions and as as R. rubrum cytochrome C2, requires multiple dele- deletions must be postulated before a match can be obtained. well. Nevertheless, these two cytochromes c2 show no better reac- tions and insertions for alignment, whereas in this report we tivity with the mitochondrial cytochrome c oxidase than do describe another group, including Rm. vannielii and Rps. the less well-matched cytochromes c2. The bearing of these viridis cytochromes c2, which require only a single residue findings on possible evolutionary relationship between mito- deletion for optimal alignment with mitochondrial cyto- chondria and prokaryotes is discussed. chrome c. The non-sulfur purple bacteria (Rhodospirtllaceae) are a family of photosynthetic prokaryotes (1) which possess char- MATERIALS AND METHODS acteristic pigments and have the same type of metabolism. Rm. vanniehi (ATCC 17100) and Rps. viridis (NTHC 133) They share a unique ability to utilize a wide range of simple were grown anaerobically in the light on modified Hutner's organic carbon sources and.some members can grow non- medium (14), and the heme and non-heme iron proteins photosynthetically under fully aerobic conditions. However, were isolated and purified by standard methods (15). In they do not exhibit a common morphology. Rhodomicro- each case the cytochrome C2 was the only soluble cyto- bium vanniehi resembles the nonphotosynthetic Hyphomi- chrome. It was isolated in a yield of about 15 ;imol/kg from crobiaceae in that daughter cells are formed as spherical Rm. vanntelii and 30 .umol/kg from Rps. viridis. buds at the ends of filaments growing out from the mother The amino-acid sequences of the cytochromes C2 were de- cell. Rhodopseudomonas viridis also uses a budding mode of termined by the methods used for other bacterial cyto- cell division, but lacks the stalked. and branched appearance chromes (16), and to similar standards. Protein (2-3 Mmol) of Rhodomicrobium. All but two of the remaining Rhodo- was treated with HgCl2 in 8 M urea/0. 1 M HC1 at 370 for 16 spirillaceae species, including rods, spirilla, and cocci, repro- hr to remove the heme, and after gel filtration and lyophili- duce through binary fission. zation the sample was digested with a protease. The peptides All Rhodospirillaceae produce large amounts of soluble formed were fractionated by gel filtration followed by high- c-type cytochrome when growing photosynthetically. The voltage paper electrophoresis and paper chromatography. best-studied example is the cytochrome C2 from Rhodospiril- Peptide sequences were investigated by the dansyl-Edman lum rubrum (2), for which both the amino-acid sequence (3) method, and by exo-and endo-peptidase digestion. The and three-dimensional structure (4) are known. R. rubrum NH2-terminal sequence of the Rm. vannielii protein was cytochrome C2 has a strong structural resemblance to mito- also investigated with an automatic sequenator (Beckman chondrial cytochrome c (5) and is more closely related in se- model 890A) (17). Amide and acid groups were assigned quence to the eukaryotic proteins than are any of the other from peptide electrophoretic mobilities, exopeptidase action, bacterial cytochromes examined (6) before now. and Staphylococcus aureus protease (18) digestion. In most species of Rhodospirillaceae, the predominant c- type cytochrome resembles R. rubrum cytochrome C2 in op- tical spectra, in oxidation-reduction potential (7), and in lim- RESULTS ited reactivity with beef heart cytochrome oxidase (8). This The amino-acid sequences of the cytochromes c2 from Rm. is true also (B. Errede and M. D. Kamen, unpublished) for vaelii and Rps. viridis are shown in Fig. 1, aligned with rep- the only soluble cytochromes found in Rm. vannielil and resentative mitochondrial cytochrome c sequences. Rps. mrldis (10). In cells of R. rubrum, the cytochrome C2 The sequence of the Rm. vannielii protein has been deter- can be photooxidized (11), but in Rps. mridis light-induced mined exhaustively. Peptides accounting for the whole of absorbance changes have been ascribed (10, 12) to a pair of the postulated sequence have been purified and character- particulate cytochromes (analogous to those of the purple ized from each of tryptic, chymotryptic, and thermolysin di- sulfur bacterium Chromatium dinosum). gests. The evidence from these peptides was not sufficient to establish the overlap at bond 97/98 (horse cytochrome num- § From whom reprints should be requested. bering), and there was only a single residue overlap at bonds 472 Downloaded by guest on September 24, 2021 Biochemistry: Ambler et al. Proc. Nat. Acad. Sci. USA 73 (1976) 473 1 5 10 15 20 Rhodomicrobium vannielii Ala Asp-Pro-Val-LysfGlyu-Gln-Val fhe -D- -Lys-Gln-Cys-Lys- Ile -Cys-His Gln-Val- Rhodopseudomonas viridis <-Glu-Asp-Ala-Ala-Ser -Gly1Glu-Gln-Val 1Phe. -D- -Lys-Gln-Cys-Lys-Val Cys-His Ser- Ile - Horse Ac fGl4Asp-Val-Glu-LysfGlyjLysys Ile jPhejVal-Gln-Lys-Cys Ala-Gln-Cys-His Thr-Val- Euglena gracilis Ac.Asp-Ala-Glu-Arg LysL LeuhGlu- Ser -Arg-Ala Ala -Gln-Cys-His. Ser -Ala- 25 30 35 40 45 Gly-Pro -Thr-Ala -Lys-Asn-Gly-Val Gly-Pro Glu -Gin -Asn-Asp-Val -Phe-Gly-Gln-Lys-Ala Gly Ala -Arg-Pro Gly Phe-Asn -Tyr Ser - Gly-Pro I Ala-Lys-Asn-Lys-Val Gly-Pro Val Leu Asn Gly Leu-Phe-Gly Arg His-Ser -Gly Thr- Ile -Glu GlyjPhe-Ser -Tyr Ser- Glu{Lys-Giy}Gly-Lys- His -Lys-ThrfGIy-Pro Asn Leu His tGIy jLeu-Phe-Gly Arg-Lys-Thr GIyFGln-Ala-Pro lylPhe-Thr Tyr Thr- GinLys-GI Val--D- -Asn- Ser -Thr ly-Pro Ser 1Trp f Val -Tyr-GlythThr-Ser Ser -Val-Pro j Tyr-Ala Ser- 50 55 60 65 70 Asp a et-Lys-Asn-Ser-Gly-Leu-ThrrpAsp-Glu-Ala -Thr~ Asp-Lys-Tyr{ §Glu Asn-Pro-Lys Ala -Val - Asp Ala-Asn Lys-Asn-Ser-Gly- Ile -Thr Trp Thr-Glu-Glu-Val-Phe-Arg-Glu-Tyr- Ile -Arg Pro-Lys Aia -Lys- Asp Ala-Asn Lys-Asn-Lys-Gly- Ile -Thr Trp Lys-Glu-Glu-Thr Leu Met-Glu-TyrfLeu4Glu Asn-Pro-Lys-Lys Tyr- Asn Ala-Asn Lys-Asn-Ala-Ala - Ile -Val Glu-Glu-Glu-Thr Leu His -Lys-Phe Leu Glu Asn-Pro-Lys-Lys Tyr- 75 80 85 90 95 100 ValiPro-GIy-Thr-Lys-Met Vai Phe Valily Leu Lys Asn-Pro-Gln-Asp A la Asp. Val Ile-Ala-Tyr Leu-Lys-Gln-Leu- Ser -Gly - Ile Pro-Gly-Thr-Lys-Met Ile Phe Ala Gly. Ile Lys Asp-Glu-Gln-Lys -Val -Ser Asp Leu Ile-Ala-Tyr Leu-Lys-Gln-Phe -Asn- Ala- Ile la Ile Leu Ile-Ala-Tyr Leu-Lys-Lys-Ala-Thr-Asn- Pro-Gly-Thr-Lys-Met Phe GIy Lys Lys-Lys-Thr-Glu Arg iu Asp Val o-Gly-Thr-Lys-Met Alafle Phe Ala Ile Ala-Lys-Lys-Asp ign As Ile ife-Ala-Tyr Met-Lys-Thr-Leu-Lys-Asp 105 Lys Asp-Gly-Ser-Lys-Lys Glu FIG. 1. Alignment of amino-acid sequences of the cytochromes c2 from Rhodomicrobium vannielii and Rhodopseudomonas viridis (this work) and mitochondrial cytochrome c from horse (20) and the alga Euglena gracilis (21, 22). The residue numbers are for the horse se- quence. The NH2-terminal residue of the Rps. viridis protein is considered to be pyrrolidone carboxylic acid. In the protein as isolated, resi- due 86 in the E. gracilis is E-N-trimethyllysine. Residues that are identical in all the four mitochondrial proteins considered in Table 1 are shown boxed, with the boxes extended if the residue is also identical in one or both of the bacterial sequences. The postulated deletions are shown as -D-. 66/67/68. However, purification and analysis of the prod- DISCUSSION ucts of CNBr cleavage of the protein provided firm evi- dence for these regions. The sequence of more than 90% of Mitochondrial cytochromes c from animals, plants, and the residues in the protein was established by the dansyl- fungi have been sequenced and a plausible phylogenetic Edman method in two or more different peptides, and exo- tree has been suggested (19). Although many bacterial c- peptidase experiments provided duplicate evidence for most type cytochromes have been sequenced (6), the cytochrome of the remaining positions.
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