Genome Analysis of the Anaerobic Thermohalophilic Bacterium Halothermothrix orenii

Halothermothirx orenii is a strictly anaerobic thermohalophilic bacterium isolated from sediment of a Tunisian salt lake. It belongs to the order Halanaerobiales in the phylum Firmicutes. The complete sequence revealed that the genome consists of one circular chromosome of 2578146 bps encoding 2451 predicted genes. This is the first genome sequence of an organism belonging to the Haloanaerobiales. Features of both Gram positive and Gram negative bacteria were identified with the presence of both a sporulating mechanism typical of Firmicutes and a characteristic Gram negative lipopolysaccharide being the most prominent. Protein sequence analyses and metabolic reconstruction reveal a unique combination of strategies for thermophilic and halophilic adaptation. H. orenii can serve as a model organism for the study of the evolution of the Gram negative phenotype as well as the adaptation under thermohalophilic conditions and the development of biotechnological applications under conditions that require high temperatures and high salt concentrations.

[1]  B. Patel,et al.  Reevaluating the classification of Halobacteroides and Haloanaerobacter species based on sequence comparisons of the 16S ribosomal RNA gene. , 1995, FEMS microbiology letters.

[2]  J. Boch,et al.  Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline , 1994, Journal of bacteriology.

[3]  T. Urich,et al.  Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane‐bound thiosulphate:quinone oxidoreductase , 2004, Molecular microbiology.

[4]  in chief George M. Garrity Bergey’s Manual® of Systematic Bacteriology , 1989, Springer New York.

[5]  T. Hansen Bergey's Manual of Systematic Bacteriology , 2005 .

[6]  L. Curatti,et al.  Sucrose metabolism: Anabaena sucrose‐phosphate synthase and sucrose‐phosphate phosphatase define minimal functional domains shuffled during evolution , 2002, FEBS letters.

[7]  影山 亜紀子,et al.  「Bergey's Manual of Systematic Bacteriology 第1版」に記載された分類とその後の分類の異同-グラム陽性菌 , 2008 .

[8]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[9]  Rainer Merkl,et al.  The genome sequence of Clostridium tetani, the causative agent of tetanus disease , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Netrusov,et al.  The catalase and superoxide dismutase genes are transcriptionally up-regulated upon oxidative stress in the strictly anaerobic archaeon Methanosarcina barkeri. , 2006, Microbiology.

[11]  G. Singer,et al.  Genomic and proteomic adaptations to growth at high temperature , 2004, Genome Biology.

[12]  Nikos Kyrpides,et al.  The Genomes On Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata , 2007, Nucleic Acids Res..

[13]  K. Matsui,et al.  Functional Analysis of the Twin-Arginine Translocation Pathway in Corynebacterium glutamicum ATCC 13869 , 2006, Applied and Environmental Microbiology.

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

[15]  I-Min A. Chen,et al.  The Genomes On Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata , 2007, Nucleic Acids Res..

[16]  I-Min A. Chen,et al.  The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions , 2007, Nucleic Acids Res..

[17]  R. Furbank,et al.  Cloning and expression of a prokaryotic sucrose-phosphate synthase gene from the cyanobacterium Synechocystis sp. PCC 6803 , 1999, Plant Molecular Biology.

[18]  Eleftherios T. Papoutsakis,et al.  A comparative genomic view of clostridial sporulation and physiology , 2005, Nature Reviews Microbiology.

[19]  B. Patel,et al.  Random sequence analysis of genomic DNA of an anaerobic, thermophilic, halophilic bacterium, Halothermothrix orenii , 2001, Extremophiles.

[20]  Maria Staiano,et al.  Proteins from extremophiles as stable tools for advanced biotechnological applications of high social interest , 2007, Journal of The Royal Society Interface.

[21]  B. Patel,et al.  Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly‐extreme condition , 2006, FEBS letters.

[22]  M. Kates,et al.  Osmometric and microscopic studies on bilayers of polar lipids from the extreme halophile, Halobacterium cutirubrum. , 1974, Biochimica et biophysica acta.

[23]  I. Kobayashi Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. , 2001, Nucleic acids research.

[24]  B. Patel,et al.  Crystal structure of the polyextremophilic alpha-amylase AmyB from Halothermothrix orenii: details of a productive enzyme-substrate complex and an N domain with a role in binding raw starch. , 2008, Journal of molecular biology.

[25]  Sean R. Eddy,et al.  Rfam: annotating non-coding RNAs in complete genomes , 2004, Nucleic Acids Res..

[26]  B. Patel,et al.  Cloning, sequencing and expression of an alpha-amylase gene, amyA, from the thermophilic halophile Halothermothrix orenii and purification and biochemical characterization of the recombinant enzyme. , 2002, Microbiology.

[27]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[28]  V. Kunin,et al.  Evolutionary conservation of sequence and secondary structures in CRISPR repeats , 2007, Genome Biology.

[29]  K. Schleifer,et al.  ARB: a software environment for sequence data. , 2004, Nucleic acids research.

[30]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[31]  B. Patel,et al.  Expression, purification and preliminary crystallographic analysis of sucrose phosphate synthase (SPS) from Halothermothrix orenii. , 2005, Acta crystallographica. Section F, Structural biology and crystallization communications.

[32]  B. Patel,et al.  Isolation and characterization of Halothermothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fermentative, strictly anaerobic bacterium. , 1994, International journal of systematic bacteriology.

[33]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[34]  M. Takeuchi,et al.  Regulatory Loop between Redox Sensing of the NADH/NAD+ Ratio by Rex (YdiH) and Oxidation of NADH by NADH Dehydrogenase Ndh in Bacillus subtilis , 2006, Journal of bacteriology.

[35]  M. Podar,et al.  New opportunities revealed by biotechnological explorations of extremophiles. , 2006, Current opinion in biotechnology.

[36]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[37]  S. Ehrlich,et al.  Two Essential DNA Polymerases at the Bacterial Replication Fork , 2001, Science.

[38]  J. Bujnicki,et al.  The Structure of Sucrose Phosphate Synthase from Halothermothrix orenii Reveals Its Mechanism of Action and Binding Mode[W][OA] , 2008, The Plant Cell Online.