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The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae.

Gross R, Guzman CA, Sebaihia M, dos Santos VA, Pieper DH, Koebnik R, Lechner M, Bartels D, Buhrmester J, Choudhuri JV, Ebensen T, Gaigalat L, Herrmann S, Khachane AN, Larisch C, Link S, Linke B, Meyer F, Mormann S, Nakunst D, Rückert C, Schneiker-Bekel S, Schulze K, Vorhölter FJ, Yevsa T, Engle JT, Goldman WE, Pühler A, Göbel UB, Goesmann A, Blöcker H, Kaiser O, Martinez-Arias R - BMC Genomics (2008)

Bottom Line: Bordetella petrii is the only environmental species hitherto found among the otherwise host-restricted and pathogenic members of the genus Bordetella.In this manuscript we present the results of the analysis of the completely annotated genome sequence of the B. petrii strain DSMZ12804.Its remarkable metabolic versatility may enable B. petrii to thrive in very different ecological niches.

View Article: PubMed Central - HTML - PubMed

Affiliation: Chair of Microbiology, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany. roy@biozentrum.uni-wuerzburg.de

ABSTRACT

Background: Bordetella petrii is the only environmental species hitherto found among the otherwise host-restricted and pathogenic members of the genus Bordetella. Phylogenetically, it connects the pathogenic Bordetellae and environmental bacteria of the genera Achromobacter and Alcaligenes, which are opportunistic pathogens. B. petrii strains have been isolated from very different environmental niches, including river sediment, polluted soil, marine sponges and a grass root. Recently, clinical isolates associated with bone degenerative disease or cystic fibrosis have also been described.

Results: In this manuscript we present the results of the analysis of the completely annotated genome sequence of the B. petrii strain DSMZ12804. B. petrii has a mosaic genome of 5,287,950 bp harboring numerous mobile genetic elements, including seven large genomic islands. Four of them are highly related to the clc element of Pseudomonas knackmussii B13, which encodes genes involved in the degradation of aromatics. Though being an environmental isolate, the sequenced B. petrii strain also encodes proteins related to virulence factors of the pathogenic Bordetellae, including the filamentous hemagglutinin, which is a major colonization factor of B. pertussis, and the master virulence regulator BvgAS. However, it lacks all known toxins of the pathogenic Bordetellae.

Conclusion: The genomic analysis suggests that B. petrii represents an evolutionary link between free-living environmental bacteria and the host-restricted obligate pathogenic Bordetellae. Its remarkable metabolic versatility may enable B. petrii to thrive in very different ecological niches.

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Overview of the degradation capacity of aromatic compounds by B. petrii. Aromatic compounds (boxed) are funneled through a variety of peripheral reactions (represented by arrows) into central intermediates, which are then processed by a central pathway to TCA cycle intermediates. However, neither salicylate nor phenylacetate could be used by B. petrii as sole source of carbon and energy (data not shown), probably due to the absence of a ferredoxin reductase encoding gene within the salicylate 5-hydroxylase encoding gene cluster (Bpet2804-2806 cluster), and an incomplete paaZ gene in the phenylacetate catabolic gene cluster (Bpet 1923–1935). 4-hydroxyphenylacetate is used as sole source of carbon and energy (data not shown), even though no gene with similarity to those encoding 4-hydroxyphenylacetate 3-hydroxylase was found in the genome (see Methods for experimental details).
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Figure 5: Overview of the degradation capacity of aromatic compounds by B. petrii. Aromatic compounds (boxed) are funneled through a variety of peripheral reactions (represented by arrows) into central intermediates, which are then processed by a central pathway to TCA cycle intermediates. However, neither salicylate nor phenylacetate could be used by B. petrii as sole source of carbon and energy (data not shown), probably due to the absence of a ferredoxin reductase encoding gene within the salicylate 5-hydroxylase encoding gene cluster (Bpet2804-2806 cluster), and an incomplete paaZ gene in the phenylacetate catabolic gene cluster (Bpet 1923–1935). 4-hydroxyphenylacetate is used as sole source of carbon and energy (data not shown), even though no gene with similarity to those encoding 4-hydroxyphenylacetate 3-hydroxylase was found in the genome (see Methods for experimental details).

Mentions: The in silico analysis of the B. petrii genome revealed an unusual metabolic capability regarding the degradation of aromatic compounds summarized in Figure 5. For the metabolisation of some of these compounds including benzoate, phthalate, 3-hydroxybenzoate, 3-hydroxyphenylacetate and 4-hydroxyphenylacetate we have obtained experimental evidence (data not shown).


The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae.

Gross R, Guzman CA, Sebaihia M, dos Santos VA, Pieper DH, Koebnik R, Lechner M, Bartels D, Buhrmester J, Choudhuri JV, Ebensen T, Gaigalat L, Herrmann S, Khachane AN, Larisch C, Link S, Linke B, Meyer F, Mormann S, Nakunst D, Rückert C, Schneiker-Bekel S, Schulze K, Vorhölter FJ, Yevsa T, Engle JT, Goldman WE, Pühler A, Göbel UB, Goesmann A, Blöcker H, Kaiser O, Martinez-Arias R - BMC Genomics (2008)

Overview of the degradation capacity of aromatic compounds by B. petrii. Aromatic compounds (boxed) are funneled through a variety of peripheral reactions (represented by arrows) into central intermediates, which are then processed by a central pathway to TCA cycle intermediates. However, neither salicylate nor phenylacetate could be used by B. petrii as sole source of carbon and energy (data not shown), probably due to the absence of a ferredoxin reductase encoding gene within the salicylate 5-hydroxylase encoding gene cluster (Bpet2804-2806 cluster), and an incomplete paaZ gene in the phenylacetate catabolic gene cluster (Bpet 1923–1935). 4-hydroxyphenylacetate is used as sole source of carbon and energy (data not shown), even though no gene with similarity to those encoding 4-hydroxyphenylacetate 3-hydroxylase was found in the genome (see Methods for experimental details).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2572626&req=5

Figure 5: Overview of the degradation capacity of aromatic compounds by B. petrii. Aromatic compounds (boxed) are funneled through a variety of peripheral reactions (represented by arrows) into central intermediates, which are then processed by a central pathway to TCA cycle intermediates. However, neither salicylate nor phenylacetate could be used by B. petrii as sole source of carbon and energy (data not shown), probably due to the absence of a ferredoxin reductase encoding gene within the salicylate 5-hydroxylase encoding gene cluster (Bpet2804-2806 cluster), and an incomplete paaZ gene in the phenylacetate catabolic gene cluster (Bpet 1923–1935). 4-hydroxyphenylacetate is used as sole source of carbon and energy (data not shown), even though no gene with similarity to those encoding 4-hydroxyphenylacetate 3-hydroxylase was found in the genome (see Methods for experimental details).
Mentions: The in silico analysis of the B. petrii genome revealed an unusual metabolic capability regarding the degradation of aromatic compounds summarized in Figure 5. For the metabolisation of some of these compounds including benzoate, phthalate, 3-hydroxybenzoate, 3-hydroxyphenylacetate and 4-hydroxyphenylacetate we have obtained experimental evidence (data not shown).

Bottom Line: Bordetella petrii is the only environmental species hitherto found among the otherwise host-restricted and pathogenic members of the genus Bordetella.In this manuscript we present the results of the analysis of the completely annotated genome sequence of the B. petrii strain DSMZ12804.Its remarkable metabolic versatility may enable B. petrii to thrive in very different ecological niches.

View Article: PubMed Central - HTML - PubMed

Affiliation: Chair of Microbiology, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany. roy@biozentrum.uni-wuerzburg.de

ABSTRACT

Background: Bordetella petrii is the only environmental species hitherto found among the otherwise host-restricted and pathogenic members of the genus Bordetella. Phylogenetically, it connects the pathogenic Bordetellae and environmental bacteria of the genera Achromobacter and Alcaligenes, which are opportunistic pathogens. B. petrii strains have been isolated from very different environmental niches, including river sediment, polluted soil, marine sponges and a grass root. Recently, clinical isolates associated with bone degenerative disease or cystic fibrosis have also been described.

Results: In this manuscript we present the results of the analysis of the completely annotated genome sequence of the B. petrii strain DSMZ12804. B. petrii has a mosaic genome of 5,287,950 bp harboring numerous mobile genetic elements, including seven large genomic islands. Four of them are highly related to the clc element of Pseudomonas knackmussii B13, which encodes genes involved in the degradation of aromatics. Though being an environmental isolate, the sequenced B. petrii strain also encodes proteins related to virulence factors of the pathogenic Bordetellae, including the filamentous hemagglutinin, which is a major colonization factor of B. pertussis, and the master virulence regulator BvgAS. However, it lacks all known toxins of the pathogenic Bordetellae.

Conclusion: The genomic analysis suggests that B. petrii represents an evolutionary link between free-living environmental bacteria and the host-restricted obligate pathogenic Bordetellae. Its remarkable metabolic versatility may enable B. petrii to thrive in very different ecological niches.

Show MeSH
Related in: MedlinePlus