Abstract
Horizontal gene transfer (HGT) is a driving force in the evolution of metabolic pathways, allowing novel enzymatic functions that provide a selective advantage to be rapidly incorporated into an organism’s physiology. Here, the role of two HGT events in the evolution of methanogenesis is described. First, the acetoclastic sub-pathway of methanogenesis is shown to have evolved via a transfer of the ackA and pta genes from a cellulolytic clostridia to a family of methanogenic archaea. Second, the system for encoding the amino acid pyrrolysine, used for the synthesis of enzymes for methanogenesis from methylamines, is shown to likely have evolved via transfer from an ancient, unknown, deeply branching organismal lineage.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Horowitz, N. H. (1945) On the evolution of biochemical syntheses. Proc Natl Acad Sci U S A 31, 153–7.
Jensen, R. A. (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30, 409–25.
Fondi, M., Brilli, M., Emiliani, G., Paffetti, D., Fani, R. (2007) The primordial metabolism: an ancestral interconnection between leucine, arginine, and lysine biosynthesis. BMC Evol Biol 7 Suppl 2, S3.
Fani, R., Brilli, M., Fondi, M., Lio, P. (2007) The role of gene fusions in the evolution of metabolic pathways: the histidine biosynthesis case. BMC Evol Biol 7 Suppl 2, S4.
Caspi, R., Foerster, H., Fulcher, C. A., Kaipa, P., Krummenacker, M., Latendresse, M., Paley, S., Rhee, S. Y., Shearer, A. G., Tissier, C., Walk, T. C., Zhang, P., Karp, P. D. (2007) The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 36, D623–31.
Dejongh, M., Formsma, K., Boillot, P., Gould, J., Rycenga, M., Best, A. (2007) Toward the automated generation of genome-scale metabolic networks in the SEED. BMC Bioinformatics 8, 139.
Pal, C., Papp, B., Lercher, M. J. (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37, 1372–5.
Chistoserdova, L., Jenkins, C., Kalyuzhnaya, M. G., Marx, C. J., Lapidus, A., Vorholt, J. A., Staley, J. T., Lidstrom, M. E. (2004) The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol Biol Evol 21, 1234–41.
Chistoserdova, L., Laukel, M., Portais, J. C., Vorholt, J. A., Lidstrom, M. E. (2004) Multiple formate dehydrogenase enzymes in the facultative methylotroph Methylobacterium extorquens AM1 are dispensable for growth on methanol. J Bacteriol 186, 22–8.
Gribaldo, S., Brochier-Armanet, C. (2006) The origin and evolution of Archaea: a state of the art. Philos Trans R Soc Lond B Biol Sci 361, 1007–22.
Bapteste, E., Brochier, C., Boucher, Y. (2005) Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1, 353–63.
Li, Q., Li, L., Rejtar, T., Lessner, D. J., Karger, B. L., Ferry, J. G. (2006) Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans. J Bacteriol 188, 702–10.
Smith, K. S., Ingram-Smith, C. (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15, 150–5.
Ferry, J. G. (1992) Methane from acetate. J Bacteriol 174, 5489–95.
Galagan, J. E., Nusbaum, C., Roy, A., Endrizzi, M. G., Macdonald, P., Fitzhugh, W., Calvo, S., Engels, R., Smirnov, S., Atnoor, D., Brown, A., Allen, N., Naylor, J., Stange-Thomann, N., Dearellano, K., Johnson, R., Linton, L., Mcewan, P., Mckernan, K., Talamas, J., Tirrell, A., Ye, W., Zimmer, A., Barber, R. D., Cann, I., Graham, D. E., Grahame, D. A., Guss, A. M., Hedderich, R., Ingram-Smith, C., Kuettner, H. C., Krzycki, J. A., Leigh, J. A., Li, W., Liu, J., Mukhopadhyay, B., Reeve, J. N., Smith, K., Springer, T. A., Umayam, L. A., White, O., White, R. H., Conway De Macario, E., Ferry, J. G., Jarrell, K. F., Jing, H., Macario, A. J., Paulsen, I., Pritchett, M., Sowers, K. R., Swanson, R. V., Zinder, S. H., Lander, E., Metcalf, W. W., Birren, B. (2002) The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12, 532–42.
Boone, D., Whitman, W., Koga, Y. (2001) Order III. Methanosarcinales, in Bergey’s Manual of Systematic Bacteriology (Boone, D., Castenholz G., Garrity G., ed.) Springer-Verlag, New York, 268–94.
Thauer, R. K. (1998) Biochemistry of metha- nogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology 144 (Pt 9), 2377–406.
Ingram-Smith, C., Martin, S. R., Smith, K. S. (2006) Acetate kinase: not just a bacterial enzyme. Trends Microbiol 14, 249–53.
White, D. (2000) The Physiology and Biochemistry of Prokaryotes, Oxford University Press, New York.
Meile, L., Rohr, L. M., Geissmann, T. A., Herensperger, M., Teuber, M. (2001) Characterization of the D-xylulose 5-phosphate/D-fructose 6-phosphate phosphoketolase gene (xfp) from Bifidobacterium lactis. J Bacteriol 183, 2929–36.
Wolfe, A. J. (2005) The acetate switch. Microbiol Mol Biol Rev 69, 12–50.
Fournier, G. P., Gogarten, J. P. (2008) Evolution of acetoclastic methanogenesis in Methanosarcina via horizontal gene transfer from cellulolytic Clostridia. J Bacteriol 190, 1124–7.
Ronquist, F., Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–4.
Felsenstein, J. (2005) PHYLIP (Phylogeny Inference Package). In Distributed by the Author. Department of Genome Sciences, University of Washington, Seattle Place.
Guindon, S., Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.
Stams, A. (1994) Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie Van Leeuwenhoek 66, 271–94.
Beiko, R. G., Harlow, T. J., Ragan, M. A. (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102, 14332–7.
Lawson, P. A., Llop-Perez, P., Hutson, R. A., Hippe, H., Collins, M. D. (1993) Towards a phylogeny of the clostridia based on 16S rRNA sequences. FEMS Microbiol Lett 113, 87–92.
Desvaux, M. (2005) Clostridium cellulolyticum: model organism of mesophilic cellulolytic clostridia. FEMS Microbiol Rev 29, 741–64.
Collins, M. D., Lawson, P. A., Willems, A., Cordoba, J. J., Fernandez-Garayzabal, J., Garcia, P., Cai, J., Hippe, H., Farrow, J. A. (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44, 812–26.
Wellman, C. H., Osterloff, P. L., Mohiuddin, U. (2003) Fragments of the earliest land plants. Nature 425, 282–5.
Min, H., Zinder, S. H. (1989) Kinetics of acetate utilization by two thermophilic acetotrophic methanogens: Methanosarcina sp. Strain CALS-1 and Methanothrix sp. Strain CALS-1. Appl Environ Microbiol 55, 488–91.
Zhang, Y., Gladyshev, V. N. (2007) High content of proteins containing 21st and 22nd amino acids, selenocysteine and pyrrolysine, in a symbiotic deltaproteobacterium of gutless worm Olavius algarvensis. Nucleic Acids Res 35, 4952–63.
Herring, S., Ambrogelly, A., Polycarpo, C. R., Soll, D. (2007) Recognition of pyrrolysine tRNA by the Desulfitobacterium hafniense pyrrolysyl-tRNA synthetase. Nucleic Acids Res 35, 1270–8.
Krzycki, J. A. (2004) Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases. Curr Opin Chem Biol 8, 484–91.
Zhang, Y., Baranov, P. V., Atkins, J. F., Gladyshev, V. N. (2005) Pyrrolysine and selenocysteine use dissimilar decoding strategies. J Biol Chem 280, 20740–51.
Polycarpo, C., Ambrogelly, A., Berube, A., Winbush, S. M., Mccloskey, J. A., Crain, P. F., Wood, J. L., Soll, D. (2004) An aminoacyl-tRNA synthetase that specifically activates pyrrolysine. Proc Natl Acad Sci U S A 101, 12450–4.
Longstaff, D. G., Blight, S. K., Zhang, L., Green-Church, K. B., Krzycki, J. A. (2007) In vivo contextual requirements for UAG translation as pyrrolysine. Mol Microbiol 63, 229–41.
Longstaff, D. G., Larue, R. C., Faust, J. E., Mahapatra, A., Zhang, L., Green-Church, K. B., Krzycki, J. A. (2007) A natural genetic code expansion cassette enables transmissible biosynthesis and genetic encoding of pyrrolysine. Proc Natl Acad Sci U S A 104, 1021–6.
Zhaxybayeva, O., Gogarten, J. P. (2004) Cladogenesis, coalescence and the evolution of the three domains of life. Trends Genet 20, 182–7.
Novichkov, P. S., Omelchenko, M. V., Gelfand, M. S., Mironov, A. A., Wolf, Y. I., Koonin, E. V. (2004) Genome-wide molecular clock and horizontal gene transfer in bacterial evolution. J Bacteriol 186, 6575–85.
Huang, J., Xu, Y., Gogarten, J. P. (2005) The presence of a haloarchaeal type tyrosyl-tRNA synthetase marks the opisthokonts as monophyletic. Mol Biol Evol 22, 2142–6.
Gogarten-Boekels, M., Hilario, E., Gogarten, J. P. (1995) The effects of heavy meteorite bombardment on the early evolution – the emergence of the three domains of life. Orig Life Evol Biosph 25, 251–64.
Gogarten, J. P., Fournier, G., Zhaxybayeva, O. (2007) Gene transfer and the reconstruction of life’s early history from genomic data. Space Sci Rev 135, 115–31.
Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–7.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Humana Press, a part of Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Fournier, G. (2009). Horizontal Gene Transfer and the Evolution of Methanogenic Pathways. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_9
Download citation
DOI: https://doi.org/10.1007/978-1-60327-853-9_9
Publisher Name: Humana Press
Print ISBN: 978-1-60327-852-2
Online ISBN: 978-1-60327-853-9
eBook Packages: Springer Protocols