Photosynthesis Research

, Volume 70, Issue 1, pp 19–41 | Cite as

The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1

  • Chris Mackenzie
  • Madhusudan Choudhary
  • Frank W. Larimer
  • Paul F. Predki
  • Stephanie Stilwagen
  • Judith P. Armitage
  • Robert D. Barber
  • Timothy J. Donohue
  • Jonathan P. Hosler
  • Jack E. Newman
  • James P. Shapleigh
  • R. Elizabeth Sockett
  • Jill Zeilstra-Ryalls
  • Samuel Kaplan
Article

Abstract

Rhodobacter sphaeroides 2.4.1 is an α-3 purple nonsulfur eubacterium with an extensive metabolic repertoire. Under anaerobic conditions, it is able to grow by photosynthesis, respiration and fermentation. Photosynthesis may be photoheterotrophic using organic compounds as both a carbon and a reducing source, or photoautotrophic using carbon dioxide as the sole carbon source and hydrogen as the source of reducing power. In addition, R. sphaeroides can grow both chemoheterotrophically and chemoautotrophically. The structural components of this metabolically diverse organism and their modes of integrated regulation are encoded by a genome of ∼4.5 Mb in size. The genome comprises two chromosomes CI and CII (2.9 and 0.9 Mb, respectively) and five other replicons. Sequencing of the genome has been carried out by two groups, the Joint Genome Institute, which carried out shotgun-sequencing of the entire genome and The University of Texas-Houston Medical School, which carried out a targeted sequencing strategy of CII. Here we describe our current understanding of the genome when data from both of these groups are combined. Previous work had suggested that the two chromosomes are equal partners sharing responsibilities for fundamental cellular processes. This view has been reinforced by our preliminary analysis of the virtually completed genome sequence. We also have some evidence to suggest that two of the plasmids, pRS241a and pRS241b encode chromosomal type functions and their role may be more than that of accessory elements, perhaps representing replicons in a transition state.

complexity flagella gene duplication genome heme biosythesis nitrogen oxide reductase scaffold sequencing sigma factors terminal oxidases 

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References

  1. Allen LN and Hanson RS (1985) Construction of broad-host range cosmid cloning vectors: Identification of genes necessary for growth of Methylobacterium organophilum on methanol. J Bacteriol 161: 955–962PubMedGoogle Scholar
  2. Armitage JP and Schmitt R (1997) Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti - variations on a theme? Microbiology 143: 3671–3682PubMedGoogle Scholar
  3. Barber RD and Donohue TJ (1998) Function of a glutathionedependent formaldehyde dehydrogenase in Rhodobacter sphaeroides, formaldehyde oxidation and assimilation. Biochemistry 37: 530–537PubMedCrossRefGoogle Scholar
  4. Brandner JP and Donohue TJ (1994) The Rhodobacter sphaeroides cytochrome c2 signal peptide is not necessary for export and heme attachment. J Bacteriol 176: 602–609PubMedGoogle Scholar
  5. Busby S and Ebright RH (1994) Promoter structure, promoter recognition and transcription activation in prokaryotes. Cell 79: 743–746PubMedCrossRefGoogle Scholar
  6. Choudhary M and Kaplan S (2000) DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28: 862–867PubMedCrossRefGoogle Scholar
  7. Choudhary M, Mackenzie C, Nereng KS, Sodergren EJ, Weinstock G and Kaplan S (1994) Multiple chromosomes in bacteria: Structure and functions of chromosome II of Rhodobacter sphaeroides 2.4.1T. J Bacteriol 176: 7694–7702PubMedGoogle Scholar
  8. Choudhary M, Mackenzie C, Nereng K, Sodergren E, Weinstock GM and Kaplan S (1997) Low-resolution sequencing of Rhodobacter sphaeroides 2.4.1T: Chromosome II is a true chromosome. Microbiology 143: 3085–99PubMedCrossRefGoogle Scholar
  9. Choudhary M, Mackenzie C, Mouncey NJ and Kaplan S (1999) RsGDB, the Rhodobacter sphaeroides Genome Database. Nucleic Acids Res 27: 61–62PubMedCrossRefGoogle Scholar
  10. Clayton RK and Sistrom WR (1978) The Photosynthetic Bacteria. Plenum Press, New YorkGoogle Scholar
  11. Dryden S and Kaplan S (1990) Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res 18: 7267–7277PubMedGoogle Scholar
  12. Dryden SC and Kaplan S (1993) Identification of cis-acting regulatory regions upstream of the rRNA operons of Rhodobacter sphaeroides. J Bacteriol 175: 6392–6402PubMedGoogle Scholar
  13. Fornari CS, Watkins M and Kaplan S (1984) Plasmid distribution and analysis in Rhodopseudomonas sphaeroides. Plasmid 11: 39–47PubMedCrossRefGoogle Scholar
  14. Galagan JE, Nusbaum C, Roy A, Endrizzi M, Macdonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stang-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye W, Zimmer A, Barber R, Cann I, Graham DE, Grahame DA, Guss A, Hedderich R, Ingram-Smith C, Kuettner HC, Krzycki JA, Leigh JA, Li W, Liu J, Mukhopadhyay B, Reeve JN, Smith K, Springer T, Umayam LA, White O, White RH, Conway de Macario E, Ferry JG, Jarrell KF, Jing H, Macario AJL, Paulsen I, Pritchett M, Sowers KR, Swanson RV, Zinder SH, Lander E, Metcalf WW and Birren B (2001) The complete genome sequence of Methanosarcina acetivorans C2A. Nature (submitted)Google Scholar
  15. Goodfellow IG, Pollitt CE and Sockett RE (1996) Cloning of the fliI gene from Rhodobacter sphaeroides WS8 by analysis of a transposon mutant with impaired motility. FEMS Microbiol Lett 142: 111–116PubMedCrossRefGoogle Scholar
  16. Gough S, Petersen B and Duus J (2000) Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97: 6908–6913PubMedCrossRefGoogle Scholar
  17. Gruber TM and Bryant DA (1997) Molecular systematic studies of eubacteria, using σ 70-type sigma factors of group 1 and group 2. J Bacteriol 179: 1734–1747PubMedGoogle Scholar
  18. Hallenbeck PL, Lerchen R, Hessler P and Kaplan S (1990a) Phosphoribulokinase activity and the regulation of CO2 fixation critical for photosynthetic growth of Rhodobacter sphaeroides.J Bacteriol 172: 1749–1761PubMedGoogle Scholar
  19. Hallenbeck PL, Lerchen R, Hessler P and Kaplan S (1990b) The role of CFXA, CFXB, and external electron acceptors in the regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase expression in Rhodobacter sphaeroides. J Bacteriol 172: 1736–1748PubMedGoogle Scholar
  20. Hamblin PA, Maguire BA, Grishanin RN and Armitage JP (1997) Evidence for two chemosensory pathways in Rhodobacter sphaeroides. Mol Microbiol 26: 1083–1096PubMedCrossRefGoogle Scholar
  21. Hamza I, Qi Z, King N and O'Brian M (2000) Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum. Microbiology 146: 669–676PubMedGoogle Scholar
  22. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Umayam L, Gill SR, Nelson KE, Read TD, Tettelin H, Richardson D, Ermolaeva MD, Vamathevan J, Bass S, Qin H, Dragoi I, Sellers P. McDonald L, Utterback T, Fleishmann RD, Nierman WC and White O (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477–483PubMedCrossRefGoogle Scholar
  23. Heusterspreute M, Thai VH, Emery S, Tournis-Gamble S, Kennedy N and Davidson J (1985) Vectors with restriction site banks. IV pJRD184, a 3793-bp plasmid vector having 43 unique cloning sites. Gene 39: 299–304PubMedCrossRefGoogle Scholar
  24. Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li BC and Herrmann R (1996) Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res 24: 4420–4449PubMedCrossRefGoogle Scholar
  25. Ielpi L, Dylan T, Ditta GS, Helinski DR and Stanfield SW (1990) The ndvB locus of Rhizobium meliloti encodes a 319-kDa protein involved in the production of beta-(1-2)-glucan. J Biol Chem 265: 2843–2851PubMedGoogle Scholar
  26. Jain R and Shapleigh JP 2001 Characterization of nirV and a gene encoding a novel pseudoazurin inRhodobacter sphaeroides 2.4.3. Microbiology 47: 2505–2515Google Scholar
  27. Jordan P (ed) (1991) Biosynthesis of Tetrapyrroles. Elsevier, AmsterdamGoogle Scholar
  28. Kansy JW and Kaplan S (1989) Purification, characterization and transcriptional analyses of RNA polymerases from Rhodobacter sphaeroides cells grown chemoheterotrophically and photoheterotrophically. J Biol Chem 264: 13751–13759PubMedGoogle Scholar
  29. Karls RK, Jin DJ and Donohue TJ (1993) Transcription properties of RNA polymerase holoenzymes isolated from the purple nonsulfur bacterium Rhodobacter sphaeroides. J Bacteriol 175: 7629–7638PubMedGoogle Scholar
  30. Karls RK, Brooks J, Rossmeissl P, Luedke J and Donohue TJ (1998) Metabolic roles of a Rhodobacter sphaeroides member of the σ 32 family. J Bacteriol 180: 10–19PubMedGoogle Scholar
  31. Karls RK, Wolf JR and Donohue TJ (1999) Activation of the cycA P2 promoter for the Rhodobacter sphaeroides cytochrome c 2 gene by the photosynthesis response regulator. Mol Microbiol 34: 822–835PubMedCrossRefGoogle Scholar
  32. Koch H-G, Winterstein C, Saribas AS, Alben JO and Daldal F, (2000) Roles of the ccoGHIS gene products in the biogenesis of the cbb 3-type cytochrome c oxidase. J Mol Biol 297: 49–65PubMedCrossRefGoogle Scholar
  33. Lai CY, Baumann L and Baumann P (1994) Amplification of trpEG: Adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci USA 91: 3819–3823PubMedCrossRefGoogle Scholar
  34. Lee WT, Terlesky KC and Tabita FR (1997) Cloning and characterization of two groESL operons of Rhodobacter sphaeroides: Transcriptional regulation of the heat-induced groESL operon. J Bacteriol 179: 487–495PubMedGoogle Scholar
  35. Lonetto M, Gribskov M and Gross CA (1992) The σ 70 family: Sequence conservation and evolutionary relationships. J Bacteriol 174: 3843–3849PubMedGoogle Scholar
  36. Lonetto MA, Brown KL, Rudd KE and Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci USA 91: 7573–7577PubMedCrossRefGoogle Scholar
  37. MacGregor BJ, Karls RK and Donohue TJ (1998) Transcription of the Rhodobacter sphaeroides cycA P1 promoter by alternate RNA polymerase holoenzymes. J Bacteriol 180: 1–9PubMedGoogle Scholar
  38. Mackenzie C, Chidambaram M, Sodergren EJ, Kaplan S and Weinstock G(1995) DNA repair mutants of Rhodobacter sphaeroides. J Bacteriol 177: 3027–3035PubMedGoogle Scholar
  39. Mackenzie C, Simmons AE and Kaplan S (1999) Multiple chromosomes in bacteria. The yin and yang of trp gene localization in Rhodobacter sphaeroides 2.4.1. Genetics 153: 525–38PubMedGoogle Scholar
  40. Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P and Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70: 85–106 (this issue).PubMedCrossRefGoogle Scholar
  41. Meijer WG and Tabita R (1992) Isolation and characterization of the nifUSVW-rpoN gene cluster from Rhodobacter sphaeroides. J Bacteriol 174: 3855–3866PubMedGoogle Scholar
  42. Moore MD and Kaplan S (1992) Identification of intrinsic highlevel resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: Characterization of tellurite, selenite and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J Bacteriol 174: 1505–1514PubMedGoogle Scholar
  43. Mouncey NJ, Choudhary M and Kaplan S (1997) Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: An essential metabolic gene function encoded on chromosome II. J Bacteriol 179: 7617–7624PubMedGoogle Scholar
  44. Mouncey NJ, Gak E, Choudhary M, Oh J-I and Kaplan S (2000) Respiratory pathways of Rhodobacter sphaeroides 2.4.1: Identi-fication and characterization of genes encoding quinol oxidases. FEMS Microbiol Lett 192: 205–210PubMedCrossRefGoogle Scholar
  45. Neidle E and Kaplan S (1992) Rhodobacter sphaeroides rdxA, a Homolog of Rhizobium meliloti fixG, Encodes a Membrane Protein Which May Bind Cytoplasmic [4Fe- 4S] Clusters. J Bacteriol 74: 6444–6454Google Scholar
  46. Neidle E and Kaplan S (1993a) Expression of the Rhodobacter sphaeroides hemA and hemT genes encoding two aminolevulinic acid synthase isozymes. J Bacteriol 175: 2292–2303PubMedGoogle Scholar
  47. Neidle E and Kaplan S (1993b) 5-Aminolevulinic acid availability and control of spectral complex formation in HemA and HemT mutants of Rhodobacter sphaeroides. J Bacteriol 175: 2304–2313PubMedGoogle Scholar
  48. Newman J, Anthony J and Donohue TJ (2001) The importance of zinc coordination for ChrR function as an anti-sigma factor.J Mol Biol 313: 485–499PubMedCrossRefGoogle Scholar
  49. Newman JD, Falkowski MJ, Schilke BA, Anthony LC and Donohue TJ (1999) The Rhodobacter sphaeroides ECF sigma factor, σ E, and the target promoters cycA P3 and rpoE P1. J Mol Biol 294: 307–320PubMedCrossRefGoogle Scholar
  50. Oh J-I, Eraso J and Kaplan S (2000) Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 182: 3081–3087PubMedCrossRefGoogle Scholar
  51. Oh J-I and Kaplan S (2000) Redox signaling:globalization of gene expression. EMBO J 19: 4237–4247PubMedCrossRefGoogle Scholar
  52. Poggio S, Aguilar C, Osorio A, Gonzalez- Pedrajo B, Dreyfus G and Camarena L (2000) σ 54 promoters control expression of genes encoding the hook and basal body complex in Rhodobacter sphaeroides.J Bacteriol 182: 5785–5792CrossRefGoogle Scholar
  53. Qi Z, Hamza I and O'Brian M (1999) Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci USA 96: 13056–13061PubMedCrossRefGoogle Scholar
  54. Roh JH and Kaplan S (2000) Genetic and phenotypic analyses of the rdx locus of Rhodobacter sphaeroides 2.4.1. J Bacteriol 182: 3475–3481PubMedCrossRefGoogle Scholar
  55. Roth J, Lawrence J and Bobik T (1996) Cobalamin (Coenzyme B12): Synthesis and biological significance. Ann Rev Microbiol 50: 137–181CrossRefGoogle Scholar
  56. Schwitner C, Sabaty M, Berna B, Cahors S and Richaud P (1998) Plasmid content and localization of the genes encoding the denitrification enzymes in two strains of Rhodobacter sphaeroides. FEMS Microbiol Lett 165: 313–321CrossRefGoogle Scholar
  57. Shah DSH, Perehinec T, Stevens SM, Aizawa S-I and Sockett RE (2000a) The flagellar filament of Rhodobacter sphaeroides: PHinduced polymorphic transitions and analysis of the fliC gene. J Bacteriol 182: 5218–5224PubMedCrossRefGoogle Scholar
  58. Shah DSH, Porter SL, Harris DC, Wadhams GH, Hamblin PA and Armitage JP (2000b) Identification of a fourth cheY gene in Rhodobacter sphaeroides and inter-species interaction within the bacterial chemotaxis signal transduction pathway.Mol Microbiol 35: 101–112PubMedCrossRefGoogle Scholar
  59. Shearer 6N, Hinsley A, Spanning RV and Spiro S (1999) Anaerobic growth of Paracoccus denitrificans requires cobalamin: Characterization of cobK and cobJ genes. J Bacteriol 181: 6907–6913PubMedGoogle Scholar
  60. Sockett RE, Goodfellow IG, Gunther G, Edge MJ and Shah DSH (1999) Properties of Rhodobacter sphaeroides flagellar motor proteins. In: Peschek GA, Loffelhardt W and Schmretterer G (eds) The Phototrophic Prokaryotes, pp 693–699. Plenum, New YorkGoogle Scholar
  61. Suwanto A and Kaplan S (1989a) Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: Genome size, fragment identification and gene localization. J Bacteriol 171: 5840–5849PubMedGoogle Scholar
  62. Suwanto A and Kaplan S (1989b) Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: Presence of two unique circular chromosomes. J Bacteriol 171: 5850–5859PubMedGoogle Scholar
  63. Suwanto A and Kaplan S (1992) Chromosome transfer in Rhodobacter sphaeroides: Hfr formation and genetic evidence for two unique circular chromosomes. J Bacteriol 174: 1135–1145PubMedGoogle Scholar
  64. Tosques IE, Shi J and Shapleigh JP (1996) Cloning and characterization of nnrR, whose product is required for the expression of proteins involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J Bacteriol 178: 4958–4964PubMedGoogle Scholar
  65. van Neil CB (1944) The culture, general physiology, morphology and classification of the non-sulfur purple and brown bacteria. Bacteriol Rev 8: 1Google Scholar
  66. Wadhams GH, Martin AC and Armitage JP (2000) Identification and localisation of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides. Mol Microbiol 36: 1222–1233PubMedCrossRefGoogle Scholar
  67. Wilson K (1989) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA and Struhl K (eds) Current Protocols in Molecular Biology, pp 24.1–24.5. Wiley Interscience, New YorkGoogle Scholar
  68. Woese 6CR (1987) Bacterial evolution. Microbiol Rev 51: 221–271Google Scholar
  69. Woese CR, Stackebrandt E, Weisburg WG, Paster BJ, Madigan MT, Fowler VJ, Hahn CM, Blanz P, Gupta R, Nealson KH and Fox GE (1984) The phylogeny of the purple bacteria: the alpha subdivision. Sys Appl Microbiol 5: 315–326Google Scholar
  70. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ and Woese CR (1985) Mitochondrial origins. Proc Nat Acad Sci USA 82: 4443–4447Google Scholar
  71. Yeliseev AA and Kaplan S (1995) A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1. J Biol Chem 270: 21167–21175PubMedCrossRefGoogle Scholar
  72. Young GM, Schmiel DH and Miller VL (1999) A new pathway for the secretion of virulence factors by bacteria: The flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA 96: 6456–6461Google Scholar
  73. Zeilstra- Ryalls JH and Kaplan S (1995) Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: The role of the fnrL gene. J Bacteriol 177: 6422–6431PubMedGoogle Scholar
  74. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533–616PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Chris Mackenzie
    • 1
  • Madhusudan Choudhary
    • 1
  • Frank W. Larimer
    • 2
  • Paul F. Predki
    • 3
  • Stephanie Stilwagen
    • 3
  • Judith P. Armitage
    • 4
  • Robert D. Barber
    • 5
  • Timothy J. Donohue
    • 6
  • Jonathan P. Hosler
    • 7
  • Jack E. Newman
    • 6
  • James P. Shapleigh
    • 8
  • R. Elizabeth Sockett
    • 9
  • Jill Zeilstra-Ryalls
    • 10
  • Samuel Kaplan
    • 11
  1. 1.Department of Microbiology and Molecular GeneticsUniversity of Texas-Houston Medical SchoolHoustonUSA
  2. 2.Life Sciences Division, 1060 Commerce ParkOak Ridge National LaboratoryOak RidgeUSA
  3. 3.DOE Joint Genome InstituteWalnut CreekUSA
  4. 4.Department of BiochemistryUniversity of OxfordOxfordUK
  5. 5.Department of Biological SciencesUniversity of Wisconsin-ParksideKenoshaUSA
  6. 6.Bacteriology DepartmentUniversity of Wisconsin-MadisonMadisonUSA
  7. 7.Department of BiochemistryUniversity of Mississippi Medical CenterJacksonUSA
  8. 8.Department of Microbiology, Wing HallCornell UniversityIthacaUSA
  9. 9.Institute of GeneticsUniversity of Nottingham, QMCNottinghamUK
  10. 10.Department of Biological SciencesOakland UniversityRochesterUSA
  11. 11.Department of Microbiology and Molecular GeneticsUniversity of Texas-Houston Medical SchoolHoustonUSA

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