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The Distribution and Evolution of C1 Transfer Enzymes and Evolution of the Planctomycetes

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Planctomycetes: Cell Structure, Origins and Biology

Abstract

When the first genome sequence of a Planctomycete became available (in 2003), it revealed the presence of genes encoding a pathway for a tetrahydromethanopterin-mediated transfer of C1 units between the oxidation levels of formaldehyde and formate, resembling a pathway for methanogenesis being carried out by a specialized group of Archaea and a pathway for formaldehyde oxidation employed by some methylotrophic bacteria, the latter pathway acting in reverse to methanogenesis. This discovery was of importance as the presence of the genes in question in the Planctomycetes has challenged the assumption of a limited distribution of these genes/pathways in the microbial world, at the same time suggesting novel scenarios for the evolution of C1 transfer pathways in microbes and providing support for the potential antiquity of these pathways. In this chapter, I review the early work on the discovery and analysis of the genetic determinants of C1 functions in Planctomycetes and the significance of these discoveries in interpreting the emergence and the evolution of C1 metabolism in Prokaryotes. This is followed by a review of the continuously emerging new genomic data suggesting a much wider distribution of the tetrahydromethanopterin-linked functions in Prokaryotes, further supporting the hypothesis of the long evolution for these functions. While the Planctomycetes provide these important insights into the evolution of specific biochemical pathways as well as the evolution of Prokaryotes in general, the exact function of the tetrahydromethanopterin-linked C1 transfer pathway in Planctomycetes and in many other phyla remains unknown.

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Abbreviations

H4MPT:

Tetrahydromethanopterin

C1:

Single carbon atom as in C1 compound, organic compound containing a single carbon atom

MtdB:

NAD(P)-linked methylene-H4MPT dehydrogenase

MFR:

Methanofuran

H4MPT:

Tetrahydromethanopterin

F420 :

Coenzyme F420

CoM:

Coenzyme M

CoB:

Coenzyme B. Fae formaldehyde-activating enzyme

MtdB MtdC:

Methylene-H4MPT dehydrogenases

Mch:

Methenyl-H4MPT cyclohydrolase

FhcABCD:

Formyltransferase/hydrolase complex

FdwD:

Is homologous to the D subunit of formyl-MFR dehydrogenase

LUCA:

Last universal common ancestor

References

  • Arrhenius T, Arrhenius G, Paplawsky W (1994) Archean geochemistry of formaldehyde and cyanide and the oligomerization of cyanohydrin. Orig Life Evol Biosph 24:1–17

    Article  PubMed  CAS  Google Scholar 

  • Bauer M, Lombardot T, Teeling H, Ward NL, Amann RI, Glöckner FO (2004) Archaea-like genes for C1-transfer enzymes in Planctomycetes: phylogenetic implications of their unexpected presence in this phylum. J Mol Evol 59:571–586

    Article  PubMed  CAS  Google Scholar 

  • Boucher Y, Douady CJ, Papke RT, Walsh DA, Boudreau MER, Nesbø C, Case RJ, Doolitle WF (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37:283–328

    Article  PubMed  CAS  Google Scholar 

  • Brochier C, Philippe H (2002) Phylogeny: a non-hyperthermophilic ancestor for bacteria. Nature 417:244

    Article  PubMed  CAS  Google Scholar 

  • Brown SD, Begemann MB, Mormile MR, Wall JD, Han CS, Goodwin LA, Pitluck S, Land ML, Hauser LJ, Elias DA (2011) Complete genome sequence of the haloalkaliphilic, hydrogen-producing bacterium Halanaerobium hydrogeniformans. J Bacteriol 193:3682–3683

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52:7–76

    PubMed  CAS  Google Scholar 

  • Chistoserdova L (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13:2603–2622

    Article  PubMed  CAS  Google Scholar 

  • Chistoserdova L, Vorholt JA, Thauer RK, Lidstrom ME (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea. Science 281:99–102

    Article  PubMed  CAS  Google Scholar 

  • Chistoserdova L, Jenkins C, Kalyuzhnaya MG, Marx CJ, Lapidus A, Vorholt JA, Staley JT, Lidstrom ME (2004) The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol Biol Evol 21:1234–1241

    Article  PubMed  CAS  Google Scholar 

  • Chistoserdova L, Lapidus A, Han C, Goodwin L, Saunders L, Brettin T, Tapia R, Gilna P, Lucas S, Richardson PM, Lidstrom ME (2007) The genome of Methylobacillus flagellatus, the molecular basis for obligate methylotrophy, and the polyphyletic origin of methylotrophy. J Bacteriol 189:4020–4027

    Article  PubMed  CAS  Google Scholar 

  • Clum A, Tindall BJ, Sikorski J, Ivanova N, Mavrommatis K, Lucas S, Glavina Del Rio T, Nolan M, Chen F, Tice H, Pitluck S, Cheng JF, Chertkov O, Brettin T, Han C, Detter JC, Kuske C, Bruce D, Goodwin L, Ovchinikova G, Pati A, Mikhailova N, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Chain P, Rohde M, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A (2009) Complete genome sequence of Pirellula staleyi type strain (ATCC 27377). Stand Genomic Sci 1:308–316

    Article  PubMed  Google Scholar 

  • DeLong EF (2000) Resolving a methane mystery. Nature 407:577

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Elshahed MS, Youssef NH, Luo Q, Najar FZ, Roe BA, Sisk TM, Bühring SI, Hinrichs KU, Krumholz LR (2007) Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma. Appl Environ Microbiol 73:4707–4716

    Article  PubMed  CAS  Google Scholar 

  • Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548

    Article  PubMed  CAS  Google Scholar 

  • Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238

    Article  PubMed  CAS  Google Scholar 

  • Göker M, Cleland D, Saunders E, Lapidus A, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng JF, Tapia R, Han C, Goodwin L, Pitluck S, Liolios K, Pagani I, Ivanova N, Mavromatis K, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Detter JC, Beck B, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2011) Complete genome sequence of Isosphaera pallida type strain (IS1B). Stand Genomic Sci 4:63–71

    Article  PubMed  Google Scholar 

  • Hagemeier CH, Chistoserdova L, Lidstrom ME, Thauer RK, Vorholt JA (2000) Characterization of a second methylene tetrahydromethanopterin dehydrogenase from Methylobacterium extorquens AM1. Eur J Biochem 267:3762–3769

    Article  PubMed  CAS  Google Scholar 

  • Kalyuzhnaya MG, Chistoserdova L (2005) Community-level analysis: genes encoding methanopterin-dependent enzymes. Meth Enzymol 397:443–454

    Article  PubMed  CAS  Google Scholar 

  • Kalyuzhnaya MG, Korotkova N, Crowther G, Marx CJ, Lidstrom ME, Chistoserdova L (2005) Analysis of gene islands involved in methanopterin-linked C1 transfer reactions reveals new functions and provides evolutionary insights. J Bacteriol 187:4607–4614

    Article  PubMed  CAS  Google Scholar 

  • Kalyuzhnaya MG, Lapidus A, Ivanova N, McHardy A, Copeland AC, Suciu D, Salamov A, McHardy A, Szeto E, Levine SR, Barry K, Green-Tringe S, Grigoriev I, Markowitz V, Rigoutsos I, Richardson PM, Lidstrom ME, Chistoserdova L (2008) High-resolution metagenomics targets major functional types in complex microbial communities. Nat Biotechnol 26:1029–1034

    Article  PubMed  CAS  Google Scholar 

  • Kane SR, Chakicherla AY, Chain PS, Schmidt R, Shin MW, Legler TC, Scow KM, Larimer FW, Lucas SM, Richardson PM, Hristova KR (2007) Whole-genome analysis of the methyl tert-butyl ether-degrading beta-proteobacterium Methylibium petroleiphilum PM1. J Bacteriol 189(5):1931–1945

    Article  PubMed  CAS  Google Scholar 

  • Kasting J, Siefert JL (2002) Life and the evolution of Earth’s atmosphere. Science 296:1066–1068

    Article  PubMed  CAS  Google Scholar 

  • Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Ann Rev Microbiol 63:31–334

    Article  Google Scholar 

  • LaButti K, Sikorski J, Schneider S, Nolan M, Lucas S, Glavina Del Rio T, Tice H, Cheng JF, Goodwin L, Pitluck S, Liolios K, Ivanova N, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Tindall BJ, Rohde M, Göker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A (2010) Complete genome sequence of Planctomyces limnophilus type strain (Mü 290). Stand Genomic Sci 3:47–56

    Article  PubMed  Google Scholar 

  • Lösekann TK, Knittel T, Nadalig B, Fuchs H, Niemann AB, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby mud volcano, Barents Sea. Appl Environ Microbiol 73:3348–3362

    Article  PubMed  Google Scholar 

  • Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil Trans R Soc Lond 358:59–83

    Article  CAS  Google Scholar 

  • Marx CJ, O'Brien BN, Breezee J, Lidstrom ME (2003) Novel methylotrophy genes of Methylobacterium extorquens AM1 identified by using transposon mutagenesis including a putative dihydromethanopterin reductase. J Bacteriol 185:669–673

    Article  PubMed  CAS  Google Scholar 

  • Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC (2012) The Genomes OnLine Database (GOLD) v. 4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 40:D571–D579

    Article  PubMed  CAS  Google Scholar 

  • Reeve JN, Nölling J, Morgan RM, Smith DR (1997) Methanogenesis: genes, genomes, and who’s on first? J Bacteriol 179:5975–5986

    PubMed  CAS  Google Scholar 

  • Sauter LM, Latypova E, Smalley NE, Lidstrom ME, Hallam S, Kalyuzhnaya MG (2012) Methanotrophic communities of Saanich Inlet: A microcosm perspective. Syst Appl Microbiol 35(3):198–203

    Article  PubMed  CAS  Google Scholar 

  • Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, Hirsch P (2004) Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. and emended description of the genus Pirellula. Int J Syst Evol Microbiol 54:1567–1580

    Article  PubMed  CAS  Google Scholar 

  • Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJ, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MS, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794

    Article  PubMed  Google Scholar 

  • Vorholt JA, Chistoserdova L, Lidstrom ME, Thauer RK (1998) The NADP-dependent methylene tetrahydromethanopterin dehydrogenase in Methylobacterium extorquens AM1. J Bacteriol 180:5351–5356

    PubMed  CAS  Google Scholar 

  • Vorholt JA, Chistoserdova L, Stolyar SM, Lidstrom ME, Thauer RK (1999) Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol 181:5750–5757

    PubMed  CAS  Google Scholar 

  • Vorholt JA, Marx CJ, Lidstrom ME, Thauer RK (2000) Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol 182(23):6645–6650

    Article  PubMed  CAS  Google Scholar 

  • Vorholt JA, Kalyuzhnaya MG, Hagemeier CH, Lidstrom ME, Chistoserdova L (2005) MtdC, a novel class of methylene tetrahydromethanopterin dehydrogenases. J Bacteriol 187:6069–6074

    Article  PubMed  CAS  Google Scholar 

  • Vuilleumier S, Chistoserdova L, Lee MC, Bringel F, Lajus A, Zhou Y, Gourion B, Barbe V, Chang J, Cruveiller S, Dossat C, Gillett W, Gruffaz C, Haugen E, Hourcade E, Levy R, Mangenot S, Muller E, Nadalig T, Pagni M, Penny C, Peyraud R, Robinson DG, Roche D, Rouy Z, Saenampechek C, Salvignol G, Vallenet D, Wu Z, Marx CJ, Vorholt JA, Olson MV, Kaul R, Weissenbach J, Médigue C, Lidstrom ME (2009) Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C1 compounds from natural and industrial sources. PLoS One 4:e5584

    Article  PubMed  Google Scholar 

  • Webster G, Sass H, Cragg BA, Gorra R, Knab NJ, Green CJ, Mathes F, Fry JC, Weightman AJ, Parkes RJ (2011) Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions. FEMS Microbiol Ecol 77:248–263

    Article  PubMed  CAS  Google Scholar 

  • Woebken D, Teeling H, Wecker P, Dumitriu A, Kostadinov I, Delong EF, Amann R, Glöckner FO (2007) Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. ISME J 1:419–435

    Article  PubMed  CAS  Google Scholar 

  • Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D'haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056–1060

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The author acknowledges support from the National Science Foundation (Grants MCB-0604269 and MCB-0950183).

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  1. Department of Chemical Engineering, University of Washington, 616 NE Northlake Place, Seattle, Washington, 98195, USA

    Ludmila Chistoserdova

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  1. Ludmila Chistoserdova
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Correspondence to Ludmila Chistoserdova .

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  1. School of Chemistry and Molecular, Biosciences, The University of Queensland, Brisbane, St. Lucia, 4072, Australia

    John A. Fuerst

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Chistoserdova, L. (2013). The Distribution and Evolution of C1 Transfer Enzymes and Evolution of the Planctomycetes. In: Fuerst, J. (eds) Planctomycetes: Cell Structure, Origins and Biology. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-502-6_8

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