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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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Comparative DNA analysis of Cupriavidus chromosomes.Nucleotide based comparison of the CHR1 replicons of the four Cupriavidus species (abbreviations as in Figure 3) and R. solanacearum GMI1000 (denoted as Rsol) using the anchor-allignment software Murasaki (http://murasaki.dna.bio.keio.ac.jp/) [218]. Scale in Mb is shown on top.
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pone-0010433-g004: Comparative DNA analysis of Cupriavidus chromosomes.Nucleotide based comparison of the CHR1 replicons of the four Cupriavidus species (abbreviations as in Figure 3) and R. solanacearum GMI1000 (denoted as Rsol) using the anchor-allignment software Murasaki (http://murasaki.dna.bio.keio.ac.jp/) [218]. Scale in Mb is shown on top.

Mentions: Full length alignment of the main replicons of the four Cupriavidus genomes and the closely related R. solanacearum genome clearly suggests a common ancestral architecture for CHR1 (Figure 4): overall homology between their respective CHR2 replicons is much lower (Figure S2) probably owing to different evolutionary histories. Such multiple alignments also reveal a large number of DNA rearrangements in the CH34 genome compared to the other analysed genomes (and vice versa), including some large inversions, and multiple sequence duplications causing significant paralogy in both CH34 replicons (discussed further). Pairwise synteny analysis using the LinePlot tool embedded in the MaGe interface fully supported these results (data not shown) while limited synteny was observed between CHR1 of C. metallidurans and the single replicons of the other organisms listed in Table 2. The intragenomic synteny between the CHR1 and CHR2 replicons of C. metallidurans was not very apparent. However, choosing a small synton size in the LinePlot analysis tool (with S≤5 e.g considering five or less genes for each synteny group), highlighted a myriad of sequence matches (data not shown). This type of local synteny may be partly explained by evolutionary DNA exchange between the two replicons or by parallel insertion of homologous sequences of incoming DNA.


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)

Comparative DNA analysis of Cupriavidus chromosomes.Nucleotide based comparison of the CHR1 replicons of the four Cupriavidus species (abbreviations as in Figure 3) and R. solanacearum GMI1000 (denoted as Rsol) using the anchor-allignment software Murasaki (http://murasaki.dna.bio.keio.ac.jp/) [218]. Scale in Mb is shown on top.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0010433-g004: Comparative DNA analysis of Cupriavidus chromosomes.Nucleotide based comparison of the CHR1 replicons of the four Cupriavidus species (abbreviations as in Figure 3) and R. solanacearum GMI1000 (denoted as Rsol) using the anchor-allignment software Murasaki (http://murasaki.dna.bio.keio.ac.jp/) [218]. Scale in Mb is shown on top.
Mentions: Full length alignment of the main replicons of the four Cupriavidus genomes and the closely related R. solanacearum genome clearly suggests a common ancestral architecture for CHR1 (Figure 4): overall homology between their respective CHR2 replicons is much lower (Figure S2) probably owing to different evolutionary histories. Such multiple alignments also reveal a large number of DNA rearrangements in the CH34 genome compared to the other analysed genomes (and vice versa), including some large inversions, and multiple sequence duplications causing significant paralogy in both CH34 replicons (discussed further). Pairwise synteny analysis using the LinePlot tool embedded in the MaGe interface fully supported these results (data not shown) while limited synteny was observed between CHR1 of C. metallidurans and the single replicons of the other organisms listed in Table 2. The intragenomic synteny between the CHR1 and CHR2 replicons of C. metallidurans was not very apparent. However, choosing a small synton size in the LinePlot analysis tool (with S≤5 e.g considering five or less genes for each synteny group), highlighted a myriad of sequence matches (data not shown). This type of local synteny may be partly explained by evolutionary DNA exchange between the two replicons or by parallel insertion of homologous sequences of incoming DNA.

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