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The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri.

Miller WG, Parker CT, Rubenfield M, Mendz GL, Wösten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G, Malek JA, Rogosin A, Stanker LH, Mandrell RE - PLoS ONE (2007)

Bottom Line: In addition, the analyses indicated also that a substantial proportion of the A. butzleri genome is devoted to growth and survival under diverse environmental conditions, with a large number of respiration-associated proteins, signal transduction and chemotaxis proteins and proteins involved in DNA repair and adaptation.The presence of pathways and loci associated often with non-host-associated organisms, as well as genes associated with virulence, suggests that A. butzleri is a free-living, water-borne organism that might be classified rightfully as an emerging pathogen.The genome sequence and analyses presented in this study are an important first step in understanding the physiology and genetics of this organism, which constitutes a bridge between the environment and mammalian hosts.

View Article: PubMed Central - PubMed

Affiliation: Produce Safety and Microbiology Research Unit, Agricultural Research Service, US Department of Agriculture, Albany, California, United States of America. bmiller@pw.usda.gov

ABSTRACT

Background: Arcobacter butzleri is a member of the epsilon subdivision of the Proteobacteria and a close taxonomic relative of established pathogens, such as Campylobacter jejuni and Helicobacter pylori. Here we present the complete genome sequence of the human clinical isolate, A. butzleri strain RM4018.

Methodology/principal findings: Arcobacter butzleri is a member of the Campylobacteraceae, but the majority of its proteome is most similar to those of Sulfuromonas denitrificans and Wolinella succinogenes, both members of the Helicobacteraceae, and those of the deep-sea vent Epsilonproteobacteria Sulfurovum and Nitratiruptor. In addition, many of the genes and pathways described here, e.g. those involved in signal transduction and sulfur metabolism, have been identified previously within the epsilon subdivision only in S. denitrificans, W. succinogenes, Sulfurovum, and/or Nitratiruptor, or are unique to the subdivision. In addition, the analyses indicated also that a substantial proportion of the A. butzleri genome is devoted to growth and survival under diverse environmental conditions, with a large number of respiration-associated proteins, signal transduction and chemotaxis proteins and proteins involved in DNA repair and adaptation. To investigate the genomic diversity of A. butzleri strains, we constructed an A. butzleri DNA microarray comprising 2238 genes from strain RM4018. Comparative genomic indexing analysis of 12 additional A. butzleri strains identified both the core genes of A. butzleri and intraspecies hypervariable regions, where <70% of the genes were present in at least two strains.

Conclusion/significance: The presence of pathways and loci associated often with non-host-associated organisms, as well as genes associated with virulence, suggests that A. butzleri is a free-living, water-borne organism that might be classified rightfully as an emerging pathogen. The genome sequence and analyses presented in this study are an important first step in understanding the physiology and genetics of this organism, which constitutes a bridge between the environment and mammalian hosts.

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Respiratory pathways in A. butzleri strain RM4018.Transfer of electrons to the menaquinone (MQ) pool is represented by blue arrows; transfer of electrons from the menaquinone pool is represented by red arrows. b- and c-type cytochromes are shaded yellow. Genes unique within the Campylobacteraceae are labeled in green. NADH:Q OR: NADH:quinone oxidoreductase; M:Q OR: malate:quinone oxidoreductase; FormDH: formate dehydrogenase; LacDH: L-lactate dehydrogenase; SulfDH: sulfur dehydrogenase; Ubi cyt c OR: Ubiquinol cytochrome c oxidoreductase; TMAO RD: TMAO reductase; NO3RD: nitrate reductase; NO2RD: nitrite reductase; FumRD: fumarate reductase; QHAmDH: quinohemoprotein amine dehydrogenase; AldDH: aldehyde dehydrogenase; PX: peroxidase; CTQ: cysteine tryptophylquinone.
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pone-0001358-g004: Respiratory pathways in A. butzleri strain RM4018.Transfer of electrons to the menaquinone (MQ) pool is represented by blue arrows; transfer of electrons from the menaquinone pool is represented by red arrows. b- and c-type cytochromes are shaded yellow. Genes unique within the Campylobacteraceae are labeled in green. NADH:Q OR: NADH:quinone oxidoreductase; M:Q OR: malate:quinone oxidoreductase; FormDH: formate dehydrogenase; LacDH: L-lactate dehydrogenase; SulfDH: sulfur dehydrogenase; Ubi cyt c OR: Ubiquinol cytochrome c oxidoreductase; TMAO RD: TMAO reductase; NO3RD: nitrate reductase; NO2RD: nitrite reductase; FumRD: fumarate reductase; QHAmDH: quinohemoprotein amine dehydrogenase; AldDH: aldehyde dehydrogenase; PX: peroxidase; CTQ: cysteine tryptophylquinone.

Mentions: A. butzleri has a full complement of genes for aerobic/microaerobic respiration including those encoding NADH:quinone oxidoreductase, ubiquinol cytochrome c oxidase, ferredoxin, cytochrome bd oxidase, cytochrome c oxidase (cbb3-type), and F1/F0 ATPase (Figure 4), but it also has limited ability for anaerobic respiration. Potential electron donors, in addition to NADH, are hydrogen, malate and formate. One large gene cluster encodes three FeNi hydrogenases with one uptake hydrogenase (hupSL) and two membrane associated proteins encoded by hydABCDF and hyaABCD, the latter two predicted to be anchored to the membrane by the b-type cytochromes HydC and HyaC, respectively. There are two formate dehydrogenases, one selenocysteine homolog and one cysteine homolog, suggesting that selenium may be important in their regulation. Also present is a malate:quinone oxidoreductase (Mqo) and a putative lactate dehydrogenase (AB0728), suggesting that lactate may be a potential electron donor. Electrons may be transferred also to the menaquinone pool through the Sox system described above, the number of electrons depending on the substrate oxidized, 2 e− for sulfite and 8 e− for sulfide.


The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri.

Miller WG, Parker CT, Rubenfield M, Mendz GL, Wösten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G, Malek JA, Rogosin A, Stanker LH, Mandrell RE - PLoS ONE (2007)

Respiratory pathways in A. butzleri strain RM4018.Transfer of electrons to the menaquinone (MQ) pool is represented by blue arrows; transfer of electrons from the menaquinone pool is represented by red arrows. b- and c-type cytochromes are shaded yellow. Genes unique within the Campylobacteraceae are labeled in green. NADH:Q OR: NADH:quinone oxidoreductase; M:Q OR: malate:quinone oxidoreductase; FormDH: formate dehydrogenase; LacDH: L-lactate dehydrogenase; SulfDH: sulfur dehydrogenase; Ubi cyt c OR: Ubiquinol cytochrome c oxidoreductase; TMAO RD: TMAO reductase; NO3RD: nitrate reductase; NO2RD: nitrite reductase; FumRD: fumarate reductase; QHAmDH: quinohemoprotein amine dehydrogenase; AldDH: aldehyde dehydrogenase; PX: peroxidase; CTQ: cysteine tryptophylquinone.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2147049&req=5

pone-0001358-g004: Respiratory pathways in A. butzleri strain RM4018.Transfer of electrons to the menaquinone (MQ) pool is represented by blue arrows; transfer of electrons from the menaquinone pool is represented by red arrows. b- and c-type cytochromes are shaded yellow. Genes unique within the Campylobacteraceae are labeled in green. NADH:Q OR: NADH:quinone oxidoreductase; M:Q OR: malate:quinone oxidoreductase; FormDH: formate dehydrogenase; LacDH: L-lactate dehydrogenase; SulfDH: sulfur dehydrogenase; Ubi cyt c OR: Ubiquinol cytochrome c oxidoreductase; TMAO RD: TMAO reductase; NO3RD: nitrate reductase; NO2RD: nitrite reductase; FumRD: fumarate reductase; QHAmDH: quinohemoprotein amine dehydrogenase; AldDH: aldehyde dehydrogenase; PX: peroxidase; CTQ: cysteine tryptophylquinone.
Mentions: A. butzleri has a full complement of genes for aerobic/microaerobic respiration including those encoding NADH:quinone oxidoreductase, ubiquinol cytochrome c oxidase, ferredoxin, cytochrome bd oxidase, cytochrome c oxidase (cbb3-type), and F1/F0 ATPase (Figure 4), but it also has limited ability for anaerobic respiration. Potential electron donors, in addition to NADH, are hydrogen, malate and formate. One large gene cluster encodes three FeNi hydrogenases with one uptake hydrogenase (hupSL) and two membrane associated proteins encoded by hydABCDF and hyaABCD, the latter two predicted to be anchored to the membrane by the b-type cytochromes HydC and HyaC, respectively. There are two formate dehydrogenases, one selenocysteine homolog and one cysteine homolog, suggesting that selenium may be important in their regulation. Also present is a malate:quinone oxidoreductase (Mqo) and a putative lactate dehydrogenase (AB0728), suggesting that lactate may be a potential electron donor. Electrons may be transferred also to the menaquinone pool through the Sox system described above, the number of electrons depending on the substrate oxidized, 2 e− for sulfite and 8 e− for sulfide.

Bottom Line: In addition, the analyses indicated also that a substantial proportion of the A. butzleri genome is devoted to growth and survival under diverse environmental conditions, with a large number of respiration-associated proteins, signal transduction and chemotaxis proteins and proteins involved in DNA repair and adaptation.The presence of pathways and loci associated often with non-host-associated organisms, as well as genes associated with virulence, suggests that A. butzleri is a free-living, water-borne organism that might be classified rightfully as an emerging pathogen.The genome sequence and analyses presented in this study are an important first step in understanding the physiology and genetics of this organism, which constitutes a bridge between the environment and mammalian hosts.

View Article: PubMed Central - PubMed

Affiliation: Produce Safety and Microbiology Research Unit, Agricultural Research Service, US Department of Agriculture, Albany, California, United States of America. bmiller@pw.usda.gov

ABSTRACT

Background: Arcobacter butzleri is a member of the epsilon subdivision of the Proteobacteria and a close taxonomic relative of established pathogens, such as Campylobacter jejuni and Helicobacter pylori. Here we present the complete genome sequence of the human clinical isolate, A. butzleri strain RM4018.

Methodology/principal findings: Arcobacter butzleri is a member of the Campylobacteraceae, but the majority of its proteome is most similar to those of Sulfuromonas denitrificans and Wolinella succinogenes, both members of the Helicobacteraceae, and those of the deep-sea vent Epsilonproteobacteria Sulfurovum and Nitratiruptor. In addition, many of the genes and pathways described here, e.g. those involved in signal transduction and sulfur metabolism, have been identified previously within the epsilon subdivision only in S. denitrificans, W. succinogenes, Sulfurovum, and/or Nitratiruptor, or are unique to the subdivision. In addition, the analyses indicated also that a substantial proportion of the A. butzleri genome is devoted to growth and survival under diverse environmental conditions, with a large number of respiration-associated proteins, signal transduction and chemotaxis proteins and proteins involved in DNA repair and adaptation. To investigate the genomic diversity of A. butzleri strains, we constructed an A. butzleri DNA microarray comprising 2238 genes from strain RM4018. Comparative genomic indexing analysis of 12 additional A. butzleri strains identified both the core genes of A. butzleri and intraspecies hypervariable regions, where <70% of the genes were present in at least two strains.

Conclusion/significance: The presence of pathways and loci associated often with non-host-associated organisms, as well as genes associated with virulence, suggests that A. butzleri is a free-living, water-borne organism that might be classified rightfully as an emerging pathogen. The genome sequence and analyses presented in this study are an important first step in understanding the physiology and genetics of this organism, which constitutes a bridge between the environment and mammalian hosts.

Show MeSH
Related in: MedlinePlus