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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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The bvgSA and kps loci of C. metallidurans CH34.Genomic region on the CHR2 replicon of C. metallidurans CH34 covering the bvgSA locus encoding a master virulence regulon (Rmet_5710, _5714, _5724) and the kps locus for synthesis and transport of capsular polysaccharides (Rmet_5729 to _5737). Relevant synteny maps are given for 11 organisms. Abbreviations: Cpin, C. pinatubonensis JMP134; Ceut, C. eutrophus H16; Ctai, C. taiwanensis; Bpet, B. petrii DSM 12804; Bbro, Bordetella bronchiseptica RB50; Paer, Pseudomonas aeruginosa PAO1; Bpar, B. parapertussis 12822; Bper, B. pertussis Tohama I; Ecol-A, avian pathogenic Escherichia coli (APEC01); Ecol-U, uripathogenic E. coli (UTI89); Ecol-K, E. coli K12. A nearby IS1088 element (Rmet_5718) is indicated with a blue rectangle in the +1 reading frame (see text).
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pone-0010433-g006: The bvgSA and kps loci of C. metallidurans CH34.Genomic region on the CHR2 replicon of C. metallidurans CH34 covering the bvgSA locus encoding a master virulence regulon (Rmet_5710, _5714, _5724) and the kps locus for synthesis and transport of capsular polysaccharides (Rmet_5729 to _5737). Relevant synteny maps are given for 11 organisms. Abbreviations: Cpin, C. pinatubonensis JMP134; Ceut, C. eutrophus H16; Ctai, C. taiwanensis; Bpet, B. petrii DSM 12804; Bbro, Bordetella bronchiseptica RB50; Paer, Pseudomonas aeruginosa PAO1; Bpar, B. parapertussis 12822; Bper, B. pertussis Tohama I; Ecol-A, avian pathogenic Escherichia coli (APEC01); Ecol-U, uripathogenic E. coli (UTI89); Ecol-K, E. coli K12. A nearby IS1088 element (Rmet_5718) is indicated with a blue rectangle in the +1 reading frame (see text).

Mentions: Another unusual feature of signal transduction in the C. metallidurans CH34 genome is the presence of an intact phosphorelay two-component system entailing a multidomain histidine-kinase sensor protein BvgS1 (Rmet_5710) and a response-transcriptional activator BvgA (Rmet_5714). This system BvgSA controls, via the transduction of environmental signals, the expression of numerous virulence- and colonization-factors in pathogenic Bordetella species [50], [151] and resembles, respectively, the EvgSA and RocSA systems in E. coli and P. aeruginosa. E. coli contains at least 37 EvgA-activated genes, including stationary-phase acid resistance genes and multidrug efflux pump genes [152], while P. aeruginosa RocA activates fimbrial adhesin genes for forming biofilms [153]. The BvgA transcriptional activator is well conserved in the four Cupriavidus species (63–68% aa identity) and B. petrii (58% aa identity), and displays a good similarity to EvgA and RocA, and to the BvgA regulators of pathogenic Bordetella species (39–45% aa identity) (all identities with minLrap >0.95). Likewise, the length and sequence of the C. metallidurans BvgS1 protein is conserved to EvgS and RocS, as well as to the BvgS sensory proteins of pathogenic Bordetella species (29–33% aa identity, minLrap 1.0). By contrast, the BvgS equivalents of B. petrii and the three other Cupriavidus strains are devoid of the large periplasmic domain spanning nearly 400 residues (Figure 6). Thus, only the BvgSA system of C. metallidurans is fully conserved in respect to the E. coli EvgSA, P. aeruginosa RocSA, and BvgSA systems of pathogenic Bordetella. Adding to the complexity of the BvgS structures in C. metallidurans and B. petrii, both have a second Bvg histidine-kinase sensor. It is called BvgS2 (encoded by Rmet_5724 and Bpet4472) and lacks the periplasmic domain. Also, in both organisms the phosphotransfer domain HPt, which is in pathogenic Bordetella part of the BvgS sensor, is an independent protein (Rmet_5713 and Bpet4470, respectively) (Figure 6). Certainly, the region spanning bvgS1 (Rmet_5710) to bvgS2 (Rmet_5724) has undergone multiple insertions and DNA rearrangements, proof of which is a nearby IS1088 copy (Rmet_5718) inserted into a defective serine protease gene (the IS element is indicated with a blue rectangle in the +1 reading frame of Figure 6).


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)

The bvgSA and kps loci of C. metallidurans CH34.Genomic region on the CHR2 replicon of C. metallidurans CH34 covering the bvgSA locus encoding a master virulence regulon (Rmet_5710, _5714, _5724) and the kps locus for synthesis and transport of capsular polysaccharides (Rmet_5729 to _5737). Relevant synteny maps are given for 11 organisms. Abbreviations: Cpin, C. pinatubonensis JMP134; Ceut, C. eutrophus H16; Ctai, C. taiwanensis; Bpet, B. petrii DSM 12804; Bbro, Bordetella bronchiseptica RB50; Paer, Pseudomonas aeruginosa PAO1; Bpar, B. parapertussis 12822; Bper, B. pertussis Tohama I; Ecol-A, avian pathogenic Escherichia coli (APEC01); Ecol-U, uripathogenic E. coli (UTI89); Ecol-K, E. coli K12. A nearby IS1088 element (Rmet_5718) is indicated with a blue rectangle in the +1 reading frame (see text).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2864759&req=5

pone-0010433-g006: The bvgSA and kps loci of C. metallidurans CH34.Genomic region on the CHR2 replicon of C. metallidurans CH34 covering the bvgSA locus encoding a master virulence regulon (Rmet_5710, _5714, _5724) and the kps locus for synthesis and transport of capsular polysaccharides (Rmet_5729 to _5737). Relevant synteny maps are given for 11 organisms. Abbreviations: Cpin, C. pinatubonensis JMP134; Ceut, C. eutrophus H16; Ctai, C. taiwanensis; Bpet, B. petrii DSM 12804; Bbro, Bordetella bronchiseptica RB50; Paer, Pseudomonas aeruginosa PAO1; Bpar, B. parapertussis 12822; Bper, B. pertussis Tohama I; Ecol-A, avian pathogenic Escherichia coli (APEC01); Ecol-U, uripathogenic E. coli (UTI89); Ecol-K, E. coli K12. A nearby IS1088 element (Rmet_5718) is indicated with a blue rectangle in the +1 reading frame (see text).
Mentions: Another unusual feature of signal transduction in the C. metallidurans CH34 genome is the presence of an intact phosphorelay two-component system entailing a multidomain histidine-kinase sensor protein BvgS1 (Rmet_5710) and a response-transcriptional activator BvgA (Rmet_5714). This system BvgSA controls, via the transduction of environmental signals, the expression of numerous virulence- and colonization-factors in pathogenic Bordetella species [50], [151] and resembles, respectively, the EvgSA and RocSA systems in E. coli and P. aeruginosa. E. coli contains at least 37 EvgA-activated genes, including stationary-phase acid resistance genes and multidrug efflux pump genes [152], while P. aeruginosa RocA activates fimbrial adhesin genes for forming biofilms [153]. The BvgA transcriptional activator is well conserved in the four Cupriavidus species (63–68% aa identity) and B. petrii (58% aa identity), and displays a good similarity to EvgA and RocA, and to the BvgA regulators of pathogenic Bordetella species (39–45% aa identity) (all identities with minLrap >0.95). Likewise, the length and sequence of the C. metallidurans BvgS1 protein is conserved to EvgS and RocS, as well as to the BvgS sensory proteins of pathogenic Bordetella species (29–33% aa identity, minLrap 1.0). By contrast, the BvgS equivalents of B. petrii and the three other Cupriavidus strains are devoid of the large periplasmic domain spanning nearly 400 residues (Figure 6). Thus, only the BvgSA system of C. metallidurans is fully conserved in respect to the E. coli EvgSA, P. aeruginosa RocSA, and BvgSA systems of pathogenic Bordetella. Adding to the complexity of the BvgS structures in C. metallidurans and B. petrii, both have a second Bvg histidine-kinase sensor. It is called BvgS2 (encoded by Rmet_5724 and Bpet4472) and lacks the periplasmic domain. Also, in both organisms the phosphotransfer domain HPt, which is in pathogenic Bordetella part of the BvgS sensor, is an independent protein (Rmet_5713 and Bpet4470, respectively) (Figure 6). Certainly, the region spanning bvgS1 (Rmet_5710) to bvgS2 (Rmet_5724) has undergone multiple insertions and DNA rearrangements, proof of which is a nearby IS1088 copy (Rmet_5718) inserted into a defective serine protease gene (the IS element is indicated with a blue rectangle in the +1 reading frame of Figure 6).

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