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Archaea-Like Genes for C1-Transfer Enzymes in Planctomycetes: Phylogenetic Implications of Their Unexpected Presence in This Phylum

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Abstract

The unexpected presence of archaea-like genes for tetrahydromethanopterin (H4MPT)-dependent enzymes in the completely sequenced genome of the aerobic marine planctomycete Pirellula sp. strain 1 (“Rhodopirellula baltica”) and in the currently sequenced genome of the aerobic freshwater planctomycete Gemmata obscuriglobus strain UQM2246 revives the discussion on the origin of these genes in the bacterial domain. We compared the genomic arrangement of these genes in Planctomycetes and methylotrophic proteobacteria and performed a phylogenetic analysis of the encoded protein sequences to address the question whether the genes have been present in the common ancestor of Bacteria and Archaea or were transferred laterally from the archaeal to the bacterial domain and therein. Although this question could not be solved using the data presented here, some constraints on the evolution of the genes involved in archaeal and bacterial H4MPT-dependent C1-transfer may be proposed: (i) lateral gene transfer (LGT) from Archaea to a common ancestor of Proteobacteria and Planctomycetes seems more likely than the presence of the genes in the common ancestor of Bacteria and Archaea; (ii) a single event of interdomain LGT can be favored over two independent events; and (iii) the archaeal donor of the genes might have been a representative of the Methanosarcinales. In the bacterial domain, the acquired genes evolved according to distinct environmental and metabolic constraints, reflected by specific rearrangements of gene order, gene recruitment, and gene duplication, with subsequent functional specialization. During the course of evolution, genes were lost from some planctomycete genomes or replaced by orthologous genes from proteobacterial lineages.

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References

  • M Allaire YG Li RE MacKenzie M Cygler (1998) ArticleTitleThe 3-D structure of a folate-dependent dehydrogenase/cyclohydrolase bifunctional enzyme at 1.5 angstrom resolution Structure 6 173–182

    Google Scholar 

  • C Brochier H Philippe (2002) ArticleTitlePhylogeny—A non-hyperthermophilic ancestor for Bacteria Nature 417 244–244

    Google Scholar 

  • L Chistoserdova S-W Chen A Lapidus ME Lidstrom (2003) ArticleTitleMethylotrophy in Methylobacterium extorquens AM1 from genomic point of view J Bacteriol 185 2980–2987 Occurrence Handle1:CAS:528:DC%2BD3sXjs1aqu7s%3D Occurrence Handle12730156

    CAS  PubMed  Google Scholar 

  • L Chistoserdova JA Vorholt RK Thauer ME Lidstrom (1998) ArticleTitleC-1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea Science 281 99–102 Occurrence Handle10.1126/science.281.5373.99 Occurrence Handle1:CAS:528:DyaK1cXksVOmsrw%3D Occurrence Handle9651254

    Article  CAS  PubMed  Google Scholar 

  • U Deppenmeier A Johann T Hartsch R Merkl RA Schmitz R Martinez-Arias A Henne A Wiezer S Baumer C Jacobi H Bruggemann T Lienard A Christmann M Bomeke S Steckel A Bhattacharyya A Lykidis R Overbeek HP Klenk RP Gunsalus HJ Fritz G Gottschalk (2002) ArticleTitleThe genome of Methanosarcina mazei: Evidence for lateral gene transfer between Bacteria and Archaea J Mol Microbiol Biotechnol 4 453–461 Occurrence Handle1:CAS:528:DC%2BD38XlsVGks7Y%3D Occurrence Handle12125824

    CAS  PubMed  Google Scholar 

  • M Di Giulio (2003) ArticleTitleThe ancestor of the Bacteria domain was a hyperthermophile J Theor Biol 224 277–283

    Google Scholar 

  • JA Fuerst (1995) ArticleTitleThe Planctomycetes—Emerging models for microbial ecology, evolution and cell biology Microbiology-UK 141 1493–1506

    Google Scholar 

  • G Garrity (2001) Bergey’s manual of systematic bacteriology Springer New York

    Google Scholar 

  • F Glöckner M Kube M Bauer H Teeling T Lombardot W Ludwig D Gade A Beck K Borzym K Heitmann R Rabus H Schlesner R Amann R Reinhardt (2003) ArticleTitleComplete genome sequence of the marine planctomycete Pirellula sp strain 1. Proc Nat Acad Sci USA 100 8298–8303

    Google Scholar 

  • GH Gonnet MA Cohen SA Benner (1994) ArticleTitleAnalysis of amino acid substitution during divergent evolution: the 400 by 400 dipeptide substitution matrix Biochem Biophys Res Commun 199 489–496

    Google Scholar 

  • W Grabarse M Vaupel JA Vorholt S Shima RK Thauer A Wittershagen G Bourenkov HD Bartunik U Ermler (1999) ArticleTitleThe crystal structure of methenyltetrahydromethanopterin cyclohydrolase from the hyperthermophilic archaeon Methanopyrus kandleri Structure 7 1257–1268

    Google Scholar 

  • CH Hagemeier L Chistoserdova ME Lidstrom RK Thauer JA Vorholt (2000) ArticleTitleCharacterization of a second methylene tetrahydromethanopterin dehydrogenase from Methylobacterium extorquens AM1 Eur J Biochem 267 3762–3769 Occurrence Handle10.1046/j.1432-1327.2000.01413.x Occurrence Handle1:CAS:528:DC%2BD3cXksVKgtbg%3D Occurrence Handle10848995

    Article  CAS  PubMed  Google Scholar 

  • JP Huelsenbeck F Ronquist (2001) ArticleTitleMRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 754–755 Occurrence Handle10.1093/bioinformatics/17.8.754 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D Occurrence Handle11524383

    Article  CAS  PubMed  Google Scholar 

  • IntegratedGenomics (GOLD: Genomes online database) Genome sequencing of Gemmata sp. str. Wal-1

  • C Jenkins JA Fuerst (2001) ArticleTitlePhylogenetic analysis of evolutionary relationships of the planctomycete division of the domain bacteria based on amino acid sequences of elongation factor Tu J Mol Evol 52 405–418

    Google Scholar 

  • S Karlin J Mrazek (2000) ArticleTitlePredicted highly expressed genes of diverse prokaryotic genomes J Bacteriol 182 5238–5250

    Google Scholar 

  • H-P Klenk A Clayton Rebecca J-F Tomb O White E Nelson Karen A Ketchum Karen J Dodson Robert M Gwinn K Hickey Erin D Peterson Jeremy L Richardson Delwood R Kerlavage Anthony E Graham David C Kyrpides Nikos D Fleischmann Robert J Quackenbush H Lee Norman G Sutton Granger S Gill F Kirkness Ewen A Dougherty Brian K McKenny D Adams Mark B Loftus S Peterson I Reich Claudia K McNeil Leslie H Badger Jonathan A Glodek L Zhou R Overbeek D Gocayne Jeannine F Weidman Janice L McDonald T Utterback D Cotton Matthew T Spriggs P Artiach P Kaine Brian M Sykes Sean W Sadow Paul A Garland Stacey M Mason Tanya J Olsen Gary M Fraser Clare O Smith Hamilton R Woese Carl JC Venter (1997) ArticleTitleThe complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus Nature 390 364–370 Occurrence Handle10.1038/37052 Occurrence Handle9389475

    Article  PubMed  Google Scholar 

  • E Konig H Schlesner P Hirsch (1984) ArticleTitleCell-wall studies on budding bacteria of the Planctomyces Pasteuria group and on a Prosthecomicrobium sp. Arch Microbiol 138 200–205

    Google Scholar 

  • J Lawrence (1999) ArticleTitleSelfish operons: The evolutionary impact of gene clustering in prokaryotes and eukaryotes Curr Opin Genet Dev 9 642–648

    Google Scholar 

  • JG Lawrence JR Roth (1996) ArticleTitleSelfish operons: Horizontal transfer may drive the evolution of gene clusters Genetics 143 1843–1860 Occurrence Handle1:CAS:528:DyaK28XlvVSqt78%3D Occurrence Handle8844169

    CAS  PubMed  Google Scholar 

  • W Liesack H Konig H Schlesner P Hirsch (1986) ArticleTitleChemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella Planctomyces group Arch Microbiol 145 361–366

    Google Scholar 

  • MR Lindsay RI Webb JA Fuerst (1997) ArticleTitlePirellulosomes: A new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula Microbiology-UK 143 739–748

    Google Scholar 

  • W Martin M Muller (1998) ArticleTitleThe hydrogen hypothesis for the first eukaryote Nature 392 37–41 Occurrence Handle10.1038/32096 Occurrence Handle1:CAS:528:DyaK1cXhvVOht74%3D Occurrence Handle9510246

    Article  CAS  PubMed  Google Scholar 

  • CJ Marx L Chistoserdova ME Lidstrom (2003) ArticleTitleFormaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway Methylobacterium extorquens AM1 J Bacteriol 185 760–768

    Google Scholar 

  • D Moreira P Lopez-Garcia (1998) ArticleTitleSymbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: The syntrophic hypothesis J Mol Evol 47 517–530

    Google Scholar 

  • A Neef R Amann H Schlesner KH Schleifer (1998) ArticleTitleMonitoring a widespread bacterial group: In situ detection of Planctomycetes with 16S rRNA-targeted probes Microbiology-UK 144 3257–3266

    Google Scholar 

  • KE Nelson RA Clayton SR Gill ML Gwinn RJ Dodson DH Haft EK Hickey LD Peterson WC Nelson KA Ketchum L McDonald TR Utterback JA Malek KD Linher MM Garrett AM Stewart MD Cotton MS Pratt CA Phillips D Richardson J Heidelberg GG Sutton RD Fleischmann JA Eisen O White SL Salzberg HO Smith JC Venter CM Fraser (1999) ArticleTitleEvidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima Nature 399 323–329 Occurrence Handle10.1038/20601 Occurrence Handle1:CAS:528:DyaK1MXjs1WnsLo%3D Occurrence Handle10360571

    Article  CAS  PubMed  Google Scholar 

  • BK Pomper O Saurel A Milon JA Vorholt (2002) ArticleTitleGeneration of formate by the formyltransferase/hydrolase complex (Fhc) from Methylobacterium extorquens AMI FEBS Lett 523 133–137

    Google Scholar 

  • BK Pomper JA Vorholt (2001) ArticleTitleCharacterization of the formyltransferase from Methylobacterium extorquens AM1 Eur J Biochem 268 4769–4775

    Google Scholar 

  • BK Pomper JA Vorholt L Chistoserdova ME Lidstrom RK Thauer (1999) ArticleTitleA methenyl tetrahydromethanopterin cyclohydrolase and a methenyl tetrahydrofolate cyclohydrolase in Methylobacterium extorquens AM1 Eur J Biochem 261 475–480 Occurrence Handle10.1046/j.1432-1327.1999.00291.x Occurrence Handle1:CAS:528:DyaK1MXislGqtr8%3D Occurrence Handle10215859

    Article  CAS  PubMed  Google Scholar 

  • F Ronquist JP Huelsenbeck (2003) ArticleTitleMrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 1572–1574 Occurrence Handle10.1093/bioinformatics/btg180 Occurrence Handle1:CAS:528:DC%2BD3sXntlKms7k%3D Occurrence Handle12912839

    Article  CAS  PubMed  Google Scholar 

  • H Schlesner C Rendsmann BJ Tindall D Gade R Rabus S Pfeiffer P Hirsch (2004) ArticleTitleTaxonomic heterogeneity within the Planctomycetales as derived by DNA/DNA-hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina the genus Blastopirellula gen. nov. as Blastopirellula marina comb, nov., and an emended description of the genus Pirellula Int J Syst Evol Microbiol . .

    Google Scholar 

  • JW Scott ME Rasche (2002) ArticleTitlePurification, overproduction, and partial characterization of beta-RFAP synthase, a key enzyme in the methanopterin biosynthesis pathway J Bacteriol 184 4442–4448 Occurrence Handle10.1128/JB.184.16.4442-4448.2002 Occurrence Handle1:CAS:528:DC%2BD38XlvV2gsrk%3D Occurrence Handle12142414

    Article  CAS  PubMed  Google Scholar 

  • M Strous JA Fuerst EHM Kramer S Logemann G Muyzer KT van de Pas-Schoonen R Webb JG Kuenen MSM Jetten (1999) ArticleTitleMissing lithotroph identified as new planctomycete Nature 400 446–449 Occurrence Handle10.1038/22749 Occurrence Handle1:CAS:528:DyaK1MXltVGnt7c%3D Occurrence Handle10440372

    Article  CAS  PubMed  Google Scholar 

  • H Teeling T Lombardot M Bauer L Ludwig FO Glöckner (2004) ArticleTitleReevaluation of the phylogenetic position of the Planctomycetes by means of concatenated ribosomal protein sequences, DNA-directed RNA polymerase subunit sequences and whole genome trees Int J Syst Evol Microbiol 54 791–801

    Google Scholar 

  • RK Thauer (1998) ArticleTitleBiochemistry of methanogenesis: A tribute to Marjory Stephenson Microbiology-UK 144 2377–2406

    Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleClustal-W—Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • JA Vorholt (2002) ArticleTitleCofactor-dependent pathways of formaldehyde oxidation in methylotrophic bacteria Arch Microbiol 178 239–249 Occurrence Handle10.1007/s00203-002-0450-2 Occurrence Handle1:CAS:528:DC%2BD38XovValt78%3D Occurrence Handle12209256

    Article  CAS  PubMed  Google Scholar 

  • JA Vorholt RK Thauer (2002) Molybdenum and tungsten enzymes in C1 metabolism Molybdenum and tungsten: Their roles in Biological processes Marcel Dekker New York 571–619

    Google Scholar 

  • JA Vorholt L Chistoserdova ME Lidstrom RK Thauer (1998) ArticleTitleThe NADP-dependent methylene tetrahydromethanopterin dehydrogenase in Methylobacterium extorquens AM1 J Bacteriol 180 5351–5356 Occurrence Handle1:CAS:528:DyaK1cXmvVWitLs%3D Occurrence Handle9765566

    CAS  PubMed  Google Scholar 

  • JA Vorholt L Chistoserdova SM Stolyar RK Thauer ME Lidstrom (1999) ArticleTitleDistribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases J Bacteriol 181 5750–5757 Occurrence Handle1:CAS:528:DyaK1MXmtFKitLw%3D Occurrence Handle10482517

    CAS  PubMed  Google Scholar 

  • JA Vorholt CJ Marx ME Lidstrom RK Thauer (2000) ArticleTitleNovel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol J Bacteriol 182 6645–6650 Occurrence Handle10.1128/JB.182.23.6645-6650.2000 Occurrence Handle1:CAS:528:DC%2BD3MXitVCnu78%3D Occurrence Handle11073907

    Article  CAS  PubMed  Google Scholar 

  • J Wang C Jenkins RI Webb JA Fuerst (2002) ArticleTitleIsolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater Appl Environ Microbiol 68 417–422 Occurrence Handle10.1128/AEM.68.1.417-422.2002 Occurrence Handle1:CAS:528:DC%2BD38Xjt1Wluw%3D%3D Occurrence Handle11772655

    Article  CAS  PubMed  Google Scholar 

  • Ward N, Butler MK, Smith RL, Fuerst JA (2003) Genome sequencing of Gemmate obscuriglobus UQM2246 http://www.tigr.org.

  • Williams TL, Moret BME (2003) An investigation of phylogenetic likelihood methods. Proceedings of the 3rd IEEE Symposium on Bioinformatics and Bioengeneering (BIBE: 03), pp 79–86

    Google Scholar 

  • www.anammox.com. Joint environmental genomics program: Genome sequencing of Candidatus “Kuenenia stuttgartiensis” Genoscope/Technical University of Munich/University of Nijmegen

Download references

Acknowledgments

Preliminary sequence data were obtained from The Institute for Genomic Research (http://www.tigr.org). Sequencing of Gemmata obscuriglobus UQM2246 and sequencing of Methylococcus capsulatus Bath were accomplished with support from DOE. The Gemmata obscuriglobus UQM2246 genome sequencing project is a collaboration between The Institute of Genomic Research and the group of John A. Fuerst at the University of Queensland, Australia. Preliminary sequence data were also obtained from the DOE Joint Genome Institute (http://www.jgi.doe.gov/). Sequencing of Burkholderia fungorum LB400 was accomplished with support from DOE. This work was supported by the Max Planck Society and the German Federal Office of Research and Education.

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Authors and Affiliations

  1. Max Planck Institute for Marine Microbiology, Microbial Genomics Group, Celsiusstrasse 1, D-28359, Bremen, Germany

    Margarete Bauer, Thierry Lombardot, Hanno Teeling & Frank O. Glöckner

  2. Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359, Bremen, Germany

    Rudolf I. Amann

  3. The Institute for Genomic Research, 9712 Medical Center Drive, Rockville, MD, 20850, USA

    Naomi L. Ward

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  1. Margarete Bauer
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  2. Thierry Lombardot
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  3. Hanno Teeling
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  4. Naomi L. Ward
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  5. Rudolf I. Amann
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  6. Frank O. Glöckner
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Correspondence to Margarete Bauer.

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Bauer, M., Lombardot, T., Teeling, H. et al. Archaea-Like Genes for C1-Transfer Enzymes in Planctomycetes: Phylogenetic Implications of Their Unexpected Presence in This Phylum. J Mol Evol 59, 571–586 (2004). https://doi.org/10.1007/s00239-004-2643-6

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