The Complete Genome of Comamonas testosteroni Reveals Its Genetic Adaptations to Changing Environments

ABSTRACT Members of the gram-negative, strictly aerobic genus Comamonas occur in various environments. Here we report the complete genome of Comamonas testosteroni strain CNB-2. Strain CNB-2 has a circular chromosome that is 5,373,643 bp long and has a G+C content of 61.4%. A total of 4,803 open reading frames (ORFs) were identified; 3,514 of these ORFs are functionally assigned to energy production, cell growth, signal transduction, or transportation, while 866 ORFs encode hypothetical proteins and 423 ORFs encode purely hypothetical proteins. The CNB-2 genome has many genes for transportation (22%) and signal transduction (6%), which allows the cells to respond and adapt to changing environments. Strain CNB-2 does not assimilate carbohydrates due to the lack of genes encoding proteins involved in glycolysis and pentose phosphate pathways, and it contains many genes encoding proteins involved in degradation of aromatic compounds. We identified 66 Tct and nine TRAP-T systems and a complete tricarboxylic acid cycle, which may allow CNB-2 to take up and metabolize a range of carboxylic acids. This nutritional bias for carboxylic acids and aromatic compounds enables strain CNB-2 to occupy unique niches in environments. Four different sets of terminal oxidases for the respiratory system were identified, and they putatively functioned at different oxygen concentrations. This study conclusively revealed at the genomic level that the genetic versatility of C. testosteroni is vital for competition with other bacteria in its special niches.

[1]  Guo-Ping Zhao,et al.  Nucleotide Sequence of Plasmid pCNB1 from Comamonas Strain CNB-1 Reveals Novel Genetic Organization and Evolution for 4-Chloronitrobenzene Degradation , 2007, Applied and Environmental Microbiology.

[2]  C. Kitts,et al.  Azorhizobium caulinodans uses both cytochrome bd (quinol) and cytochrome cbb3 (cytochrome c) terminal oxidases for symbiotic N2 fixation , 1996, Journal of bacteriology.

[3]  Milton H. Saier,et al.  Protein Secretion and Membrane Insertion Systems in Gram-Negative Bacteria , 2006, The Journal of Membrane Biology.

[4]  Fan Yang,et al.  TIGRFAMs: a protein family resource for the functional identification of proteins , 2001, Nucleic Acids Res..

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

[6]  H. Nothaft,et al.  Sugar uptake and utilisation in Streptomyces coelicolor: a PTS view to the genome , 2000, Antonie van Leeuwenhoek.

[7]  J. S. Parkinson.  Signal transduction schemes of bacteria , 1993, Cell.

[8]  Eduardo Díaz,et al.  Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. , 2002, Environmental microbiology.

[9]  T. Kudo,et al.  Identification of 9,17-Dioxo-1,2,3,4,10,19-Hexanorandrostan-5-oic Acid, 4-Hydroxy-2-Oxohexanoic Acid, and 2-Hydroxyhexa-2,4-Dienoic Acid and Related Enzymes Involved in Testosterone Degradation in Comamonas testosteroni TA441 , 2005, Applied and Environmental Microbiology.

[10]  Long-Fei Wu,et al.  Involvement of the twin‐arginine translocation system in protein secretion via the type II pathway , 2001, The EMBO journal.

[11]  T. Kudo,et al.  A New Bacterial Steroid Degradation Gene Cluster in Comamonas testosteroni TA441 Which Consists of Aromatic-Compound Degradation Genes for Seco-Steroids and 3-Ketosteroid Dehydrogenase Genes , 2003, Applied and Environmental Microbiology.

[12]  J. Ramos,et al.  Proteomic Analysis Reveals the Participation of Energy- and Stress-Related Proteins in the Response of Pseudomonas putida DOT-T1E to Toluene , 2005, Journal of bacteriology.

[13]  C. Anthony,et al.  Roles for enteric d-type cytochrome oxidase in N2 fixation and microaerobiosis , 1990, Journal of bacteriology.

[14]  Wen‐Ming Chen,et al.  Comamonas odontotermitis sp. nov., isolated from the gut of the termite Odontotermes formosanus. , 2007, International journal of systematic and evolutionary microbiology.

[15]  J. Gardy,et al.  Genome-wide identification of Pseudomonas aeruginosa exported proteins using a consensus computational strategy combined with a laboratory-based PhoA fusion screen. , 2005, Genome research.

[16]  B. Berks,et al.  Sec-independent Protein Translocation in Escherichia coli , 1999, The Journal of Biological Chemistry.

[17]  A. Pugsley,et al.  The general secretory pathway of Klebsiella oxytoca: no evidence for relocalization or assembly of pilin‐like PulG protein into a multiprotein complex , 1993, Molecular microbiology.

[18]  Luke E. Ulrich,et al.  One-component systems dominate signal transduction in prokaryotes. , 2005, Trends in microbiology.

[19]  S. Salzberg,et al.  Optimized multiplex PCR: efficiently closing a whole-genome shotgun sequencing project. , 1999, Genomics.

[20]  Ann C. Grimm,et al.  Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene , 1997, Applied and environmental microbiology.

[21]  K. Nelson,et al.  Global features of the Pseudomonas putida KT2440 genome sequence. , 2002, Environmental microbiology.

[22]  Jigang Han,et al.  Plant-microbe association for rhizoremediation of chloronitroaromatic pollutants with Comamonas sp. strain CNB-1. , 2007, Environmental microbiology.

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

[24]  Narmada Thanki,et al.  CDD: a conserved domain database for interactive domain family analysis , 2006, Nucleic Acids Res..

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

[26]  Frank Sargent,et al.  The Tat protein translocation pathway and its role in microbial physiology. , 2003, Advances in microbial physiology.

[27]  S. Lory,et al.  Complete genome sequence of Pseudomonas aeruginosa PAO 1 , an opportunistic pathogen , 2000 .

[28]  J. Liautard,et al.  Different Roles of the Two High-Oxygen-Affinity Terminal Oxidases of Brucella suis: Cytochrome c Oxidase, but Not Ubiquinol Oxidase, Is Required for Persistence in Mice , 2006, Infection and Immunity.

[29]  T. Kudo,et al.  Arrangement and regulation of the genes for meta-pathway enzymes required for degradation of phenol in Comamonas testosteroni TA441. , 2000, Microbiology.

[30]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[31]  M. Saier,et al.  Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. , 1998, Advances in microbial physiology.

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

[33]  V. Korolik,et al.  Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori , 2000, Archives of Microbiology.

[34]  T. Kudo,et al.  Steroid degradation gene cluster of Comamonas testosteroni consisting of 18 putative genes from meta-cleavage enzyme gene tesB to regulator gene tesR. , 2004, Biochemical and biophysical research communications.

[35]  Michael Y. Galperin,et al.  Novel domains of the prokaryotic two-component signal transduction systems. , 2001, FEMS microbiology letters.

[36]  H. Hennecke,et al.  A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum , 1996, Journal of bacteriology.

[37]  J. G. Kuenen,et al.  Expression of copA and cusA in Shewanella during copper stress. , 2008, Microbiology.

[38]  B. Pettersson,et al.  Comamonas denitrificans sp. nov., an efficient denitrifying bacterium isolated from activated sludge. , 2001, International journal of systematic and evolutionary microbiology.

[39]  D. Richardson,et al.  Properties of the periplasmic nitrate reductases from Paracoccus pantotrophus and Escherichia coli after growth in tungsten-supplemented media. , 2003, FEMS microbiology letters.

[40]  P. Brennan,et al.  The genome of Mycobacterium leprae: a minimal mycobacterial gene set , 2001, Genome Biology.

[41]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[42]  Hiroyuki Ogata,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 1999, Nucleic Acids Res..

[43]  J. Stock,et al.  Signal transduction in bacteria , 1990, Nature.

[44]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

[45]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[46]  I. Zhulin,et al.  PAS domain S-boxes in Archaea, Bacteria and sensors for oxygen and redox. , 1997, Trends in biochemical sciences.

[47]  T. Mizuno,et al.  Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. , 1997, DNA research : an international journal for rapid publication of reports on genes and genomes.

[48]  M. Bally,et al.  GSP-dependent protein secretion in gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. , 1998, FEMS microbiology reviews.

[49]  S. Lory,et al.  Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen , 2000, Nature.

[50]  P. Green,et al.  Consed: a graphical tool for sequence finishing. , 1998, Genome research.

[51]  M. Aral,et al.  Comamonas testosteroni bacteremia in a patient with perforated acute appendicitis. Short communication. , 2007, Acta microbiologica et immunologica Hungarica.

[52]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[53]  K. Yoshida,et al.  Genome analysis of Agrobacterium tumefaciens: linkage map and genetic features of the left region of the linear chromosome. , 2001, Genes & genetic systems.

[54]  Zhipei Liu,et al.  Novel Partial Reductive Pathway for 4-Chloronitrobenzene and Nitrobenzene Degradation in Comamonas sp. Strain CNB-1 , 2006, Applied and Environmental Microbiology.

[55]  René L. Warren,et al.  The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse , 2006, Proceedings of the National Academy of Sciences.

[56]  R. Jain,et al.  Chemotaxis of a Ralstonia sp. SJ98 toward co-metabolizable nitroaromatic compounds. , 2002, Biochemical and biophysical research communications.

[57]  R. Poole,et al.  Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air , 1990, Journal of bacteriology.