Abstract
Psychrophilic archaea are abundant and perform critical roles throughout the Earth's expansive cold biosphere. Here we report the first complete genome sequence for a psychrophilic methanogenic archaeon, Methanococcoides burtonii. The genome sequence was manually annotated including the use of a five-tiered evidence rating (ER) system that ranked annotations from ER1 (gene product experimentally characterized from the parent organism) to ER5 (hypothetical gene product) to provide a rapid means of assessing the certainty of gene function predictions. The genome is characterized by a higher level of aberrant sequence composition (51%) than any other archaeon. In comparison to hyper/thermophilic archaea, which are subject to selection of synonymous codon usage, M. burtonii has evolved cold adaptation through a genomic capacity to accommodate highly skewed amino-acid content, while retaining codon usage in common with its mesophilic Methanosarcina cousins. Polysaccharide biosynthesis genes comprise at least 3.3% of protein coding genes in the genome, and Cell wall, membrane, envelope biogenesis COG genes are overrepresented. Likewise, signal transduction (COG category T) genes are overrepresented and M. burtonii has a high ‘IQ’ (a measure of adaptive potential) compared to many methanogens. Numerous genes in these two overrepresented COG categories appear to have been acquired from ɛ- and δ-Proteobacteria, as do specific genes involved in central metabolism such as a novel B form of aconitase. Transposases also distinguish M. burtonii from other archaea, and their genomic characteristics indicate they have an important role in evolving the M. burtonii genome. Our study reveals a capacity for this model psychrophile to evolve through genome plasticity (including nucleotide skew, horizontal gene transfer and transposase activity) that enables adaptation to the cold, and to the biological and physical changes that have occurred over the last several thousand years as it adapted from a marine to an Antarctic lake environment.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Ashby MK . (2006). Distribution, structure and diversity of ‘bacterial’ genes encoding two-component proteins in the Euryarchaeota. Archaea 2: 11–30.
Azad RK, Lawrence JG . (2007). Detecting laterally transferred genes: use of entropic clustering methods and genome position. Nucleic Acids Res 35: 4629–4639.
Boucher Y . (2007). Lipids: biosynthesis, function and evolution. In: Cavicchioli R (ed). Archaea: Molecular and Cellular Biology. ASM Press: Washington, DC, pp 341–353.
Bowman JP, Rea SM, McCammon SA, McMeekin TA . (2000). Diversity and community structure within anoxic sediments from marine salinity meromictic lakes and a coastal meromictic marine basin. Vestfold Hills, Eastern Antarctica. Environ Microbiol 2: 227–237.
Butler ECV, Burton HR, Smith JD . (1988). Iodine distribution in an Antarctic meromictic saline lake. Hydrobiologia 165: 97–101.
Cavicchioli R . (2006). Cold adapted Archaea. Nat Rev Microbiol 4: 331–343.
Cavicchioli R, DeMaere M, Thomas T . (2007). Metagenomic studies reveal the critical and wide-ranging ecological importance of uncultivated archaea: the role of ammonia oxidizers. BioEssays 29: 11–14.
Chain PSG, Denef VJ, Konstantinidis KT, Vergez LM, Agullo L, Reyes VL et al. (2006). Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 103: 15280–15287.
Chong SC, Liu Y, Cummins M, Valentine DL, Boone DR . (2002). Methanogenium marinum sp. nov., a H2-using methanogen from Skan Bay, Alaska, and kinetics of H2 utilization. Antonie Van Leeuwenhoek 81: 263–270.
Coolen MJL, Hopmans EC, Rijpstra WIC, Muyzer G, Schouten S, Volkman JK et al. (2004). Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental changes. Org Geochem 35: 1151–1167.
Costa J, Empadinhas N, Gonçalves L, Lamosa P, Santos H, da Costa MS . (2006). Characterization of the biosynthetic pathway of glucosylglycerate in the archaeon Methanococcoides burtonii. J Bacteriol 188: 1022–1030.
Cromer L, Gibson JAE, Swadling KTM, David RA . (2005). Faunal microfossils: indicators of Holocene ecological change in a saline Antarctic lake. Palaeogeogr Palaeoclimatol Palaeoecol 221: 83–97.
Dell’Anno A, Danovaro R . (2005). Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309: 2179.
DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U et al. (2006). Community genomics among stratified microbial assemblages in the ocean's interior. Science 311: 496–503.
Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R et al. (2002). The genome of Methanosarcina mazei: evidence for lateral gene transfer between Bacteria and Archaea. J Mol Microbiol Biotechnol 4: 453–461.
Enault F, Suhre K, Abergel C, Poirot O, Claverie JM . (2003). Annotation of bacterial genomes using improved phylogenomic profiles. Bioinformatics 19: i105–i107.
Fournier GP, Gogarten JP . (2008). Evolution of acetoclastic methanogenesis in Methanosarcina via horizontal gene transfer from cellulolytic Clostridia. J Bacteriol 190: 1124–1127.
Franzmann PD, Liu Y, Balkwill DL, Aldrich HC, Conway de Macario E, Boone DR . (1997). Methanogenium frigidum sp. nov., a psychrophilic, H2-using methanogen from Ace Lake, Antarctica. Int J Syst Bacteriol 47: 1068–1072.
Franzmann PD, Springer N, Ludwig W, Conway de Macario E, Rohde M . (1992). A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst. Appl Microbiol 15: 573–581.
Freeman TC, Goldovsky L, Brosch M, van Dongen S, Mazière P, Grocock RJ et al. (2007). Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput Biol 3: 2032–2042.
Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P, FitzHugh W et al. (2002). The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12: 532–542.
Galperin MY . (2005). A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35.
Galperin MY . (2006). Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188: 4169–4182.
Goodchild A, Raftery M, Saunders NFW, Guilhaus M, Cavicchioli R . (2004a). Biology of the cold adapted archaeon, Methanococcoides burtonii determined by proteomics using liquid chromatography-tandem mass spectrometry. J Proteome Res 3: 1164–1176.
Goodchild A, Raftery M, Saunders NFW, Guilhaus M, Cavicchioli R . (2005). Cold adaptation of the Antarctic archaeon, Methanococcoides burtonii assessed by proteomics using ICAT. J Proteome Res 4: 473–480.
Goodchild A, Saunders NFW, Ertan H, Raftery M, Guilhaus M, Curmi PMG . (2004b). A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol Microbiol 53: 309–321.
Grochowski LL, Xu H, White RH . (2006). Methanocaldococcus jannaschii uses a modified mevalonate pathway for biosynthesis of isopentenyl diphosphate. J Bacteriol 188: 3192–3198.
Guss AM, Mukhopadhyay B, Zhang JK, Metcalf WW . (2005). Genetic analysis of mch mutants in two Methanosarcina species demonstrates multiple roles for the methanopterin-dependent C-1 oxidation/reduction pathway and differences in H(2) metabolism between closely related species. Mol Microbiol 55: 1671–1680.
Huson DH, Auch AF, Qi J, Schuster SC . (2007). MEGAN analysis of metagenomic data. Genome Res 17: 377–386.
Ihaka R, Gentleman R . (1996). R: a language for data analysis and graphics. J Comp Graph Stat 5: 299–314.
Ivanova NN, Mavromatis K, Chen I-MA, Markowitz VM, Kyrpide NC . (2007). Standard operating procedure for the annotations of genomes and metagenomes submitted to the integrated microbial genomes expert review (IMG-ER) system. Available:http://imgweb.jgi-psf.org/w/doc/img_er_ann.pdf.
Jahn U, Summons RE, Sturt H, Grosjean E, Huber H . (2004). Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/1. Arch Microbiol 182: 404–413.
Johnson EF, Mukhopadhyay B . (2005). A new type of sulfite reductase, a novel coenzyme F420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii. J Biol Chem 280: 38776–38786.
Karcher U, Schroder H, Haslinger E, Allmaier G, Schreiner R, Wieland F et al. (1993). Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus. J Biol Chem 268: 26821–26826.
Kendall MM, Wardlaw GD, Tang CF, Bonin AS, Liu Y, Valentine DA . (2007). Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl Environ Microbiol 73: 407–414.
Klotz MG, Arp DJ, Chain PSG, El-Sheikh AF, Hauser LJ, Hommes NG et al. (2006). Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environ Microbiol 72: 6299–6315.
Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA . (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543–546.
Kotsyurbenko OR, Friedrich MW, Simankova MV, Nozhevnikova AN, Golyshin PN, Timmis KN et al. (2007). Shift from acetoclastic to H2-dependent methanogenesis in a west Siberian peat bog at low pH values and isolation of an acidophilic Methanobacterium strain. Appl Environ Microbiol 73: 2344–2348.
Kruger M, Treude T, Wolters H, Nauhaus K, Boetius A . (2005). Microbial methane turnover in different marine habitats. Palaeogeogr Palaeoclimatol Palaeoecol 227: 6–17.
Lauro FM, Tran K, Vezzi A, Vitulo N, Valle G, Bartlett DG . (2008). Large-scale transposon mutagenesis of Photobacterium profundum SS9 reveals new genetic loci important for growth at low temperature and high pressure. J Bacteriol 190: 1699–1709.
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806–809.
Li F, Hagemeier CH, Seedorf H, Gottschalk G, Thauer RK . (2007a). Re-citrate synthase from Clostridium kluyveri is phylogenetically related to homocitrate synthase and isopropylmalate synthase rather than to Si-citrate synthase. J Bacteriol 189: 4299–4304.
Li L, Kato C, Horikoshi K . (1999). Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar Biotechnol 1: 391–400.
Li L, Li Q, Rohlin L, Kim U, Salmon K, Rejtar T et al. (2007b). Quantitative proteomic and microarray analysis of the Archaeon Methanosarcina acetivorans grown with acetate versus methanol. J Proteome Res 6: 759–771.
Longstaff DG, Larue RC, Faust JE, Mahapatra A, Zhang L, Green-Church KB et al. (2007). A natural genetic code expansion cassette enables transmissible biosynthesis and genetic encoding of pyrrolysine. Proc Natl Acad Sci USA 104: 1021–1026.
Lynn DJ, Singer GAC, Hickey DA . (2002). Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res 30: 4272–4277.
Maeder DL, Anderson I, Brettin TS, Bruce DC, Gilna P, Han CS et al. (2006). The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes. J Bacteriol 188: 7922–7931.
Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN et al. (2005). Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15: 1325–1335.
Methé BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X et al. (2005). The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102: 10913–10918.
Meuer J, Kuettner HC, Zhang JK, Hedderich R, Metcalf WW . (2002). Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferridoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA 99: 5632–5637.
Moran JJ, House CH, Vrentas JM, Freeman KH . (2008). Methyl sulfide production by a novel carbon monoxide metabolism in Methanosarcina acetivorans. Appl Environ Microbiol 74: 540–542.
Morozova D, Wagner D . (2007). Stress response of methanogenic archaea from Siberian permafrost compared with methanogens from nonpermafrost habitats. FEMS Microbiol Ecol 61: 16–25.
Murakami M, Shibuya K, Nakayama T, Nishino T, Yoshimura T, Hemmi H . (2007). Geranylgeranyl reductase involved in the biosynthesis of archaeal membrane lipids in the hyperthermophilic archaeon Archaeoglobus fulgidus. FEBS J 274: 805–814.
Murray AE, Grzymski JJ . (2007). Diversity and genomics of Antarctic marine microorganisms. Phil Trans R Soc B 362: 2259–2271.
Narita S-I, Kanamaru K, Matsuyama S-I, Tokuda H . (2003). A mutation in the membrane subunit of an ABC transporter LolCDE complex causing outer membrane localization of lipoproteins against their inner membrane-specific signals. Mol Microbiol 49: 167–177.
Nichols DS, Miller MR, Davies NW, Goodchild A, Raftery M, Cavicchioli R . (2004). Cold adaptation in the Antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186: 8508–8515.
Noon KR, Guymon R, Crain PF, McCloskey JA, Thomm M, Cavicchioli R . (2003). Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature [Topt], 23 degrees C) and Stetteria hydrogenophila (Topt, 95 degrees C). J Bacteriol 185: 5483–5490.
Paramonov NA, Parolis LAS, Parolis H, Boan IF, Anton J, Rodriguez-Valera F . (1998). The structure of the exocellular polysaccharide produced by the archaeon Haloferax gibbonsii (ATCC 33959). Carbohydr Res 309: 89–94.
Parolis H, Parolis LAS, Boan IF, Rodriguez-Valera F, Widmalm G, Manca MC et al. (1996). The structure of the exopolysaccharide produced by the halophilic archaeon Haloferax mediterranei strain R4 (ATCC 33500). Carbohydr Res 295: 147–156.
Peden J . (2000). CodonW. Available:http://codonw.sourceforge.net/.
Phelps TJ, Conrad R, Zeikus JG . (1985). Sulfate-dependent interspecies H2 transfer between Methanosarcina barkeri and Desulfovibrio vulgaris during coculture metabolism of acetate or methanol. Appl Environ Microbiol 50: 589–594.
Purdy KJ, Nedwell DB, Embley TM . (2003). Analysis of the sulfate-reducing bacterial and methanogenic archaeal populations in contrasting Antarctic sediments. Appl Environ Microbiol 69: 3181–3191.
Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M et al. (2004). The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6: 887–902.
Rankin LM, Gibson JAE, Franzmann PD, Burton HR . (1999). The chemical stratification and microbial communities of Ace Lake, Antarctica: a review of the characteristics of a marine-derived meromictic lake. Polarforschung 66: 33–52.
Raymond J, Siefert JL, Staples CR, Blankenship RE . (2004). The natural history of nitrogen fixation. Mol Biol Evol 21: 541–554.
Reid IN, Sparks WB, Lubnow S, McGrath M, Livio M, Valenti J et al. (2006). Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures. Int J Astrobiol 5: 89–97.
Riley M, Staley JT, Danchin A, Wang TZ, Brettin TS, Hauser LJ et al. (2008). Genomics of an extreme psychrophile, Psychromonas ingrahamii. BMC Genomics 9: 210.
Rodriguez-Brito B, Rohwer F, Edwards RA . (2006). An application of statistics to comparative metagenomics. BMC Bioinformatics 7: 162.
Saitou N, Nei M . (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
Sato T, Atomi H, Imanaka T . (2007). Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315: 1003–1006.
Sauerwald A, Zhu W, Major TA, Roy H, Palioura S, Jahn D et al. (2005). RNA-dependent cysteine biosynthesis in archaea. Science 307: 1969–1972.
Saunders NFW, Goodchild A, Raftery M, Guilhaus M, Curmi PMG, Cavicchioli R . (2005). Predicted roles for hypothetical proteins in the low-temperature expressed proteome of the Antarctic archaeon Methanoccoides burtonii. J Proteome Res 4: 464–472.
Saunders NFW, Thomas T, Curmi PMG, Mattick JS, Kuczek E, Slade R et al. (2003). Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea, Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13: 1580–1588.
Simankova MV, Parshina SN, Tourova TP, Kolganova TV, Zehnder AJ, Nozhevnikova AN . (2001). Methanosarcina lacustris sp. nov., a new psychrotolerant methanogenic archaeon from anoxic lake sediments. Syst Appl Microbiol 24: 362–367.
Singh N, Kendall MM, Liu Y, Boone DR . (2005). Isolation and characterization of methylotrophic methanogens from anoxic marine sediments in Skan Bay, Alaska: description of Methanococcoides alakenese sp. nov., and emended description of Methanosarcina baltica. Int J Syst Evol Microbiol 55: 2531–2538.
Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM . (2007). Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318: 1449–1452.
Tallant TC, Krzycki JA . (1997). Methylthiol:Coenzyme M methyltransferase from Methanosarcina barkeri, an enzyme of methanogenesis from dimethylsulfide and methylmercaptopropionate. J Bacteriol 179: 6902–6911.
Tallant TC, Paul L, Krzycki JA . (2001). The MtsA subunit of the methylthiol:coenzyme M methyltransferase of Methanosarcina barkeri catalyses both half-reactions of corrinoid-dependent dimethylsulfide: coenzyme M methyl transfer. J Biol Chem 276: 4485–4493.
Tamura K, Dudley J, Nei M, Kumar S . (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
Thomas T, Kumar N, Cavicchioli R . (2001). Effects of ribosomes and intracellular solutes on activities and stabilities of elongation factor 2 proteins from psychrotolerant and thermophilic methanogens. J Bacteriol 183: 1974–1982.
Thompson JD, Higgins DG, Gibson TJ . (1994). CLUSTAL 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.
Tsirigos A, Rigoutsos I . (2005). A new computational method for the detection of horizontal gene transfer events. Nucleic Acids Res 33: 922–933.
Vernikos GS, Parkhill J . (2006). Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196–2203.
von Klein D, Arab H, Völker H, Thomm M . (2002). Methanosarcina baltica sp. nov., a novel methanogen isolated from the Gotland Deep of the Baltic Sea. Extremophiles 6: 103–110.
Acknowledgements
The Australian contingent was supported by funding from the Australian Research Council. The work of IJA, NI, ED, MM, AL, LH and ML was performed under the auspices of the US Department of Energy's Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under Contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, Los Alamos National Laboratory under Contract No. DE-AC02-06NA25396, and Los Alamos National Laboratory under Contract No. DE-AC05-00OR22725. The work of KRS was supported by funding from the US Department of Energy's Office of Science, Biological and Environmental Research Program Grant No. DE-FG02-07ER64502 and the National Science Foundation, Division of Cellular and Bioscience Grant No. MCB0110762. MYG was supported by the NIH Intramural Research Program at the National Library of Medicine.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website (http://www.nature.com/ismej)
Rights and permissions
About this article
Cite this article
Allen, M., Lauro, F., Williams, T. et al. The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. ISME J 3, 1012–1035 (2009). https://doi.org/10.1038/ismej.2009.45
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2009.45
Keywords
This article is cited by
-
Mediative Mechanism of Freezing/Thawing on Greenhouse Gas Emissions in an Inland Saline-Alkaline Wetland: a Metagenomic Analysis
Microbial Ecology (2023)
-
Genome-based characterization of the deep-sea psychrotolerant bacterium Bacillus altitudinis SORB11 isolated from the Indian Sector of the Southern Ocean
Polar Biology (2023)
-
Himalayan Microbiomes for Agro-environmental Sustainability: Current Perspectives and Future Challenges
Microbial Ecology (2022)
-
Remarkably coherent population structure for a dominant Antarctic Chlorobium species
Microbiome (2021)
-
Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
Microbiome (2020)
