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The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments.

Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Médigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M - PLoS ONE (2010)

Bottom Line: This tolerance is mostly achieved by rapid ion efflux but also by metal-complexation and -reduction.One out of five proteins is associated with either transport or transcription while the relay of environmental stimuli is governed by more than 600 signal transduction systems.The CH34 genome is most similar to the genomes of other Cupriavidus strains by correspondence between the respective CHR1 replicons but also displays similarity to the genomes of more distantly related species as a result of gene transfer and through the presence of large genomic islands.

View Article: PubMed Central - PubMed

Affiliation: Molecular and Cellular Biology, Belgian Nuclear Research Center SCK*CEN, Mol, Belgium. pjanssen@sckcen.be

ABSTRACT
Many bacteria in the environment have adapted to the presence of toxic heavy metals. Over the last 30 years, this heavy metal tolerance was the subject of extensive research. The bacterium Cupriavidus metallidurans strain CH34, originally isolated by us in 1976 from a metal processing factory, is considered a major model organism in this field because it withstands milli-molar range concentrations of over 20 different heavy metal ions. This tolerance is mostly achieved by rapid ion efflux but also by metal-complexation and -reduction. We present here the full genome sequence of strain CH34 and the manual annotation of all its genes. The genome of C. metallidurans CH34 is composed of two large circular chromosomes CHR1 and CHR2 of, respectively, 3,928,089 bp and 2,580,084 bp, and two megaplasmids pMOL28 and pMOL30 of, respectively, 171,459 bp and 233,720 bp in size. At least 25 loci for heavy-metal resistance (HMR) are distributed over the four replicons. Approximately 67% of the 6,717 coding sequences (CDSs) present in the CH34 genome could be assigned a putative function, and 9.1% (611 genes) appear to be unique to this strain. One out of five proteins is associated with either transport or transcription while the relay of environmental stimuli is governed by more than 600 signal transduction systems. The CH34 genome is most similar to the genomes of other Cupriavidus strains by correspondence between the respective CHR1 replicons but also displays similarity to the genomes of more distantly related species as a result of gene transfer and through the presence of large genomic islands. The presence of at least 57 IS elements and 19 transposons and the ability to take in and express foreign genes indicates a very dynamic and complex genome shaped by evolutionary forces. The genome data show that C. metallidurans CH34 is particularly well equipped to live in extreme conditions and anthropogenic environments that are rich in metals.

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Functional distribution over CHR1 and CHR2 by COG classification.The scale represents the normalised ratio of CDS numbers per replicon (i.e. the ratio of percentages for each class per replicon); a ration of 1 means that genes classified in a particular COG are, numberwise, evenly distributed over both replicons, taking into account the different total count of genes per replicon. Detailed data are in Table S1.
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pone-0010433-g002: Functional distribution over CHR1 and CHR2 by COG classification.The scale represents the normalised ratio of CDS numbers per replicon (i.e. the ratio of percentages for each class per replicon); a ration of 1 means that genes classified in a particular COG are, numberwise, evenly distributed over both replicons, taking into account the different total count of genes per replicon. Detailed data are in Table S1.

Mentions: The distribution over the replicons of the genome's functional content also was analyzed using the MaGe system. As expected, the main replicon CHR1 carries most of the essential housekeeping genes, including those needed for DNA replication, DNA repair, cell division, transcription and translation, along with sets of genes required for protein processing, folding, and post-translational modification (Figure 2; Table S1). However, a bias towards particular COG classes was also seen for the smaller replicon (classes I, K, N, Q, and T). These functional classes generally point to adaptation and survival in terms of energy storage and responsive cellular behavior. In addition, the CHR2 replicon contains several genes paralogous to CHR1 genes. Most notably are dbpA (Rmet_5284) encoding a second ATP-dependent RNA helicase, a second excinuclease gene uvrA2 (Rmet_4549), a third copy of an exodeoxyribonuclease gene xthA3 (Rmet_4910), a second glutamate dehydrogenase gene gdhA2 (Rmet_5114), a second elongation factor G encoded by fusA2 (Rmet_5930), a second translation initiation factor IF-1 encoded by infA2 (Rmet_5176), a second housekeeping sigma-70 factor encoded by rpoD2 (Rmet_4661) and six genes that code for alternative sigma factors fliA (Rmet_3702), sigJ (Rmet_3844), rpoK (Rmet_4001), rpoJ (Rmet_4499), rpoQ (Rmet_4686), and rpoM (Rmet_5400) - see also dedicated subsection on transcription factors. Furthermore, the CHR2 replicon harbours many genes and gene casettes involved in specialised metabolic- and biosynthetic-activities and adaptive responses, including those involved in carotenoid biosynthesis (carX, Rmet_5644; crtB, Rmet_4149), acetone utilisation and tolerance (acxRABC, Rmet_4104-07), polyhydroxyalkanoic acid (PHA) synthesis and conversion (phaZ, phaZ3, phaB3, phaC3), sulfonate/taurine transport and utilisation (asfRAB, tauABC, tauD, tauE), sulfite oxidation (sorAB), squalene/hopene synthesis (sqhC, Rmet_4148), tannin degradation (tanA, Rmet_3841), biofilm formation (pelABCDEFG), and exopolysaccharide synthesis (epsAPB). It carries most of the genes for motility and chemotaxis (mot, flh, fli, flg, cpa, tad, pil, fim, and che loci), peroxide removal and oxidative stress (yhjA, ahpC, ahpD, katG, pcaCD, soxR, glrX), DNA adenine methylation (dam), DNA repair (ada, alkA, alkB1, alkB2, sbcCD, ogt2, ogt3), adaptive mutagenesis (imuA-imuB-dnaE2, Rmet_4128-29-30), and eight copies of the uspA gene (two of which are located on transposons) encoding the universal stress protein [most genes and loci without Rmet numbers are also discussed in separate sections]. The CHR2 replicon also carries an intact master two-component phosphorelay system (bvgSA) that, in Bordetella species, controls hundreds of genes involved in an extensive variety of responses and physiological functions, including virulence, biofilm formation, chemotaxis, and motility [50].


The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments.

Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Médigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M - PLoS ONE (2010)

Functional distribution over CHR1 and CHR2 by COG classification.The scale represents the normalised ratio of CDS numbers per replicon (i.e. the ratio of percentages for each class per replicon); a ration of 1 means that genes classified in a particular COG are, numberwise, evenly distributed over both replicons, taking into account the different total count of genes per replicon. Detailed data are in Table S1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2864759&req=5

pone-0010433-g002: Functional distribution over CHR1 and CHR2 by COG classification.The scale represents the normalised ratio of CDS numbers per replicon (i.e. the ratio of percentages for each class per replicon); a ration of 1 means that genes classified in a particular COG are, numberwise, evenly distributed over both replicons, taking into account the different total count of genes per replicon. Detailed data are in Table S1.
Mentions: The distribution over the replicons of the genome's functional content also was analyzed using the MaGe system. As expected, the main replicon CHR1 carries most of the essential housekeeping genes, including those needed for DNA replication, DNA repair, cell division, transcription and translation, along with sets of genes required for protein processing, folding, and post-translational modification (Figure 2; Table S1). However, a bias towards particular COG classes was also seen for the smaller replicon (classes I, K, N, Q, and T). These functional classes generally point to adaptation and survival in terms of energy storage and responsive cellular behavior. In addition, the CHR2 replicon contains several genes paralogous to CHR1 genes. Most notably are dbpA (Rmet_5284) encoding a second ATP-dependent RNA helicase, a second excinuclease gene uvrA2 (Rmet_4549), a third copy of an exodeoxyribonuclease gene xthA3 (Rmet_4910), a second glutamate dehydrogenase gene gdhA2 (Rmet_5114), a second elongation factor G encoded by fusA2 (Rmet_5930), a second translation initiation factor IF-1 encoded by infA2 (Rmet_5176), a second housekeeping sigma-70 factor encoded by rpoD2 (Rmet_4661) and six genes that code for alternative sigma factors fliA (Rmet_3702), sigJ (Rmet_3844), rpoK (Rmet_4001), rpoJ (Rmet_4499), rpoQ (Rmet_4686), and rpoM (Rmet_5400) - see also dedicated subsection on transcription factors. Furthermore, the CHR2 replicon harbours many genes and gene casettes involved in specialised metabolic- and biosynthetic-activities and adaptive responses, including those involved in carotenoid biosynthesis (carX, Rmet_5644; crtB, Rmet_4149), acetone utilisation and tolerance (acxRABC, Rmet_4104-07), polyhydroxyalkanoic acid (PHA) synthesis and conversion (phaZ, phaZ3, phaB3, phaC3), sulfonate/taurine transport and utilisation (asfRAB, tauABC, tauD, tauE), sulfite oxidation (sorAB), squalene/hopene synthesis (sqhC, Rmet_4148), tannin degradation (tanA, Rmet_3841), biofilm formation (pelABCDEFG), and exopolysaccharide synthesis (epsAPB). It carries most of the genes for motility and chemotaxis (mot, flh, fli, flg, cpa, tad, pil, fim, and che loci), peroxide removal and oxidative stress (yhjA, ahpC, ahpD, katG, pcaCD, soxR, glrX), DNA adenine methylation (dam), DNA repair (ada, alkA, alkB1, alkB2, sbcCD, ogt2, ogt3), adaptive mutagenesis (imuA-imuB-dnaE2, Rmet_4128-29-30), and eight copies of the uspA gene (two of which are located on transposons) encoding the universal stress protein [most genes and loci without Rmet numbers are also discussed in separate sections]. The CHR2 replicon also carries an intact master two-component phosphorelay system (bvgSA) that, in Bordetella species, controls hundreds of genes involved in an extensive variety of responses and physiological functions, including virulence, biofilm formation, chemotaxis, and motility [50].

Bottom Line: This tolerance is mostly achieved by rapid ion efflux but also by metal-complexation and -reduction.One out of five proteins is associated with either transport or transcription while the relay of environmental stimuli is governed by more than 600 signal transduction systems.The CH34 genome is most similar to the genomes of other Cupriavidus strains by correspondence between the respective CHR1 replicons but also displays similarity to the genomes of more distantly related species as a result of gene transfer and through the presence of large genomic islands.

View Article: PubMed Central - PubMed

Affiliation: Molecular and Cellular Biology, Belgian Nuclear Research Center SCK*CEN, Mol, Belgium. pjanssen@sckcen.be

ABSTRACT
Many bacteria in the environment have adapted to the presence of toxic heavy metals. Over the last 30 years, this heavy metal tolerance was the subject of extensive research. The bacterium Cupriavidus metallidurans strain CH34, originally isolated by us in 1976 from a metal processing factory, is considered a major model organism in this field because it withstands milli-molar range concentrations of over 20 different heavy metal ions. This tolerance is mostly achieved by rapid ion efflux but also by metal-complexation and -reduction. We present here the full genome sequence of strain CH34 and the manual annotation of all its genes. The genome of C. metallidurans CH34 is composed of two large circular chromosomes CHR1 and CHR2 of, respectively, 3,928,089 bp and 2,580,084 bp, and two megaplasmids pMOL28 and pMOL30 of, respectively, 171,459 bp and 233,720 bp in size. At least 25 loci for heavy-metal resistance (HMR) are distributed over the four replicons. Approximately 67% of the 6,717 coding sequences (CDSs) present in the CH34 genome could be assigned a putative function, and 9.1% (611 genes) appear to be unique to this strain. One out of five proteins is associated with either transport or transcription while the relay of environmental stimuli is governed by more than 600 signal transduction systems. The CH34 genome is most similar to the genomes of other Cupriavidus strains by correspondence between the respective CHR1 replicons but also displays similarity to the genomes of more distantly related species as a result of gene transfer and through the presence of large genomic islands. The presence of at least 57 IS elements and 19 transposons and the ability to take in and express foreign genes indicates a very dynamic and complex genome shaped by evolutionary forces. The genome data show that C. metallidurans CH34 is particularly well equipped to live in extreme conditions and anthropogenic environments that are rich in metals.

Show MeSH
Related in: MedlinePlus