TY - JOUR

T1 - The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii

T2 - The role of genome evolution in cold adaptation

AU - Allen, Michelle A.

AU - Lauro, Federico M.

AU - Williams, Timothy J.

AU - Burg, Dominic

AU - Siddiqui, Khawar S.

AU - De Francisci, Davide

AU - Chong, Kevin W.Y.

AU - Pilak, Oliver

AU - Chew, Hwee H.

AU - De Maere, Matthew Z.

AU - Ting, Lily

AU - Katrib, Marilyn

AU - Ng, Charmaine

AU - Sowers, Kevin R.

AU - Galperin, Michael Y.

AU - Anderson, Iain J.

AU - Dalin, Eileen

AU - Martinez, Michele

AU - Lapidus, Alla

AU - Hauser, Loren

AU - Land, Miriam

AU - Thomas, Torsten

AU - Cavicchioli, Ricardo

N1 - Funding Information: 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.

PY - 2009/9

Y1 - 2009/9

N2 - 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 - and -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.

AB - 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 - and -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.

KW - Archaea

KW - Cold adaptation

KW - Genome plasticity

KW - Methanococcoides burtonii

KW - Psychrophile

UR - http://www.scopus.com/inward/record.url?scp=70349456541&partnerID=8YFLogxK

U2 - 10.1038/ismej.2009.45

DO - 10.1038/ismej.2009.45

M3 - Article

C2 - 19404327

AN - SCOPUS:70349456541

VL - 3

SP - 1012

EP - 1035

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 9

ER -