The Genome Sequence of the Crenarchaeon Acidilobus saccharovorans Supports a New Order, Acidilobales, and Suggests an Important Ecological Role in Terrestrial Acidic Hot Springs

ABSTRACT Acidilobus saccharovorans is an anaerobic, organotrophic, thermoacidophilic crenarchaeon isolated from a terrestrial hot spring. We report the complete genome sequence of A. saccharovorans, which has permitted the prediction of genes for Embden-Meyerhof and Entner-Doudoroff pathways and genes associated with the oxidative tricarboxylic acid cycle. The electron transfer chain is branched with two sites of proton translocation and is linked to the reduction of elemental sulfur and thiosulfate. The genomic data suggest an important role of the order Acidilobales in thermoacidophilic ecosystems whereby its members can perform a complete oxidation of organic substrates, closing the anaerobic carbon cycle.

[1]  E. Bonch‐Osmolovskaya,et al.  Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. , 2009, International journal of systematic and evolutionary microbiology.

[2]  J. Lobry Asymmetric substitution patterns in the two DNA strands of bacteria. , 1996, Molecular biology and evolution.

[3]  T. Friedrich,et al.  The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane‐bound multisubunit hydrogenases , 2000, FEBS letters.

[4]  Philip Hinchliffe,et al.  Structure of the Hydrophilic Domain of Respiratory Complex I from Thermus thermophilus , 2006, Science.

[5]  Luke E. Ulrich,et al.  The complete genome sequence of Staphylothermus marinus reveals differences in sulfur metabolism among heterotrophic Crenarchaeota , 2009, BMC Genomics.

[6]  J. Holden,et al.  Citric Acid Cycle in the Hyperthermophilic Archaeon Pyrobaculum islandicum Grown Autotrophically, Heterotrophically, and Mixotrophically with Acetate , 2006, Journal of bacteriology.

[7]  E. Bonch‐Osmolovskaya,et al.  Acidilobus aceticus gen. nov., sp. nov., a novel anaerobic thermoacidophilic archaeon from continental hot vents in Kamchatka. , 2000, International journal of systematic and evolutionary microbiology.

[8]  P. A. Rea,et al.  A thermostable vacuolar‐type membrane pyrophosphatase from the archaeon Pyrobaculum aerophilum: implications for the origins of pyrophosphate‐energized pumps , 1999, FEBS letters.

[9]  N. Ravin,et al.  Complete Genome Sequence of the Anaerobic, Protein-Degrading Hyperthermophilic Crenarchaeon Desulfurococcus kamchatkensis , 2008, Journal of bacteriology.

[10]  C. Sensen,et al.  Reconstruction of the Central Carbohydrate Metabolism of Thermoproteus tenax by Use of Genomic and Biochemical Data , 2004, Journal of bacteriology.

[11]  S. Salzberg,et al.  Improved microbial gene identification with GLIMMER. , 1999, Nucleic acids research.

[12]  R. Fleischmann,et al.  The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus , 1997, Nature.

[13]  S. Brunak,et al.  Improved prediction of signal peptides: SignalP 3.0. , 2004, Journal of molecular biology.

[14]  Gertraud Burger,et al.  AutoFACT: An Automatic Functional Annotation and Classification Tool , 2005, BMC Bioinformatics.

[15]  E. Boyd,et al.  Isolation, Characterization, and Ecology of Sulfur-Respiring Crenarchaea Inhabiting Acid-Sulfate-Chloride-Containing Geothermal Springs in Yellowstone National Park , 2007, Applied and Environmental Microbiology.

[16]  Peter F. Hallin,et al.  RNAmmer: consistent and rapid annotation of ribosomal RNA genes , 2007, Nucleic acids research.

[17]  B. Tjaden,et al.  The central carbohydrate metabolism of the hyperthermophilic crenarchaeote Thermoproteus tenax: pathways and insights into their regulation , 2008, Archives of Microbiology.

[18]  N. Ravin,et al.  Metabolic Versatility and Indigenous Origin of the Archaeon Thermococcus sibiricus, Isolated from a Siberian Oil Reservoir, as Revealed by Genome Analysis , 2009, Applied and Environmental Microbiology.

[19]  K. Hallberg,et al.  Carbon, iron and sulfur metabolism in acidophilic micro-organisms. , 2009, Advances in microbial physiology.

[20]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[21]  K. Suzuki,et al.  Caldisphaera lagunensis gen. nov., sp. nov., a novel thermoacidophilic crenarchaeote isolated from a hot spring at Mt Maquiling, Philippines. , 2003, International journal of systematic and evolutionary microbiology.

[22]  P. Schönheit,et al.  Oxidation of organic compounds to CO2 with sulfur or thiosulfate as electron acceptor in the anaerobic hyperthermophilic archaea Thermoproteus tenax and Pyrobaculum islandicum proceeds via the citric acid cycle , 1994, Archives of Microbiology.

[23]  E. Jayamani,et al.  Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria , 2007, Journal of bacteriology.

[24]  C. Schleper,et al.  Genome sequence of Picrophilus torridus and its implications for life around pH 0 , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  B. Berks,et al.  Specificity of respiratory pathways involved in the reduction of sulfur compounds by Salmonella enterica. , 2002, Microbiology.

[26]  H. Huber,et al.  A sodium ion‐dependent A1AO ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus , 2007, The FEBS journal.

[27]  Dmitrij Frishman,et al.  The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum , 2000, Nature.

[28]  Michael W. W. Adams,et al.  Insights into the Metabolism of Elemental Sulfur by the Hyperthermophilic Archaeon Pyrococcus furiosus: Characterization of a Coenzyme A- Dependent NAD(P)H Sulfur Oxidoreductase , 2007, Journal of bacteriology.

[29]  L. Sazanov,et al.  Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. , 2007, Biochemistry.

[30]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[31]  A Grigoriev,et al.  Analyzing genomes with cumulative skew diagrams. , 1998, Nucleic acids research.