Genomic island excisions in <it>Bordetella petrii</it>

<p>Abstract</p> <p>Background</p> <p>Among the members of the genus <it>Bordetella B. petrii </it>is unique, since it is the only species isolated from the environment, while the pathogenic Bordetellae are obligately associated with host organisms. Another f...

Full description

Bibliographic Details
Main Authors: Levillain Erwan, Hubans Christine, Hot David, Bauer Susanne, Schmitt Karin, Lechner Melanie, Locht Camille, Lemoine Yves, Gross Roy
Format: Article
Language:English
Published: BMC 2009-07-01
Series:BMC Microbiology
Online Access:http://www.biomedcentral.com/1471-2180/9/141
_version_ 1819177956394663936
author Levillain Erwan
Hubans Christine
Hot David
Bauer Susanne
Schmitt Karin
Lechner Melanie
Locht Camille
Lemoine Yves
Gross Roy
author_facet Levillain Erwan
Hubans Christine
Hot David
Bauer Susanne
Schmitt Karin
Lechner Melanie
Locht Camille
Lemoine Yves
Gross Roy
author_sort Levillain Erwan
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Among the members of the genus <it>Bordetella B. petrii </it>is unique, since it is the only species isolated from the environment, while the pathogenic Bordetellae are obligately associated with host organisms. Another feature distinguishing <it>B. petrii </it>from the other sequenced Bordetellae is the presence of a large number of mobile genetic elements including several large genomic regions with typical characteristics of genomic islands collectively known as integrative and conjugative elements (ICEs). These elements mainly encode accessory metabolic factors enabling this bacterium to grow on a large repertoire of aromatic compounds.</p> <p>Results</p> <p>During <it>in vitro </it>culture of <it>Bordetella petrii </it>colony variants appear frequently. We show that this variability can be attributed to the presence of a large number of metastable mobile genetic elements on its chromosome. In fact, the genome sequence of <it>B. petrii </it>revealed the presence of at least seven large genomic islands mostly encoding accessory metabolic functions involved in the degradation of aromatic compounds and detoxification of heavy metals. Four of these islands (termed GI1 to GI3 and GI6) are highly related to ICE<it>clc </it>of <it>Pseudomonas knackmussii </it>sp. strain B13. Here we present first data about the molecular characterization of these islands. We defined the exact borders of each island and we show that during standard culture of the bacteria these islands get excised from the chromosome. For all but one of these islands (GI5) we could detect circular intermediates. For the <it>clc</it>-like elements GI1 to GI3 of <it>B. petrii </it>we provide evidence that tandem insertion of these islands which all encode highly related integrases and attachment sites may also lead to incorporation of genomic DNA which originally was not part of the island and to the formation of huge composite islands. By integration of a tetracycline resistance cassette into GI3 we found this island to be rather unstable and to be lost from the bacterial population within about 100 consecutive generations. Furthermore, we show that GI3 is self transmissible and by conjugation can be transferred to <it>B. bronchiseptica </it>thus proving it to be an active integrative and conjugative element</p> <p>Conclusion</p> <p>The results show that phenotypic variation of <it>B. petrii </it>is correlated with the presence of genomic islands. Tandem integration of related islands may contribute to island evolution by the acquisition of genes originally belonging to the bacterial core genome. In conclusion, <it>B. petrii </it>appears to be the first member of the genus in which horizontal gene transfer events have massively shaped its genome structure.</p>
first_indexed 2024-12-22T21:34:53Z
format Article
id doaj.art-1e3fa3f0fee6406f9e3244ea5803bde3
institution Directory Open Access Journal
issn 1471-2180
language English
last_indexed 2024-12-22T21:34:53Z
publishDate 2009-07-01
publisher BMC
record_format Article
series BMC Microbiology
spelling doaj.art-1e3fa3f0fee6406f9e3244ea5803bde32022-12-21T18:11:47ZengBMCBMC Microbiology1471-21802009-07-019114110.1186/1471-2180-9-141Genomic island excisions in <it>Bordetella petrii</it>Levillain ErwanHubans ChristineHot DavidBauer SusanneSchmitt KarinLechner MelanieLocht CamilleLemoine YvesGross Roy<p>Abstract</p> <p>Background</p> <p>Among the members of the genus <it>Bordetella B. petrii </it>is unique, since it is the only species isolated from the environment, while the pathogenic Bordetellae are obligately associated with host organisms. Another feature distinguishing <it>B. petrii </it>from the other sequenced Bordetellae is the presence of a large number of mobile genetic elements including several large genomic regions with typical characteristics of genomic islands collectively known as integrative and conjugative elements (ICEs). These elements mainly encode accessory metabolic factors enabling this bacterium to grow on a large repertoire of aromatic compounds.</p> <p>Results</p> <p>During <it>in vitro </it>culture of <it>Bordetella petrii </it>colony variants appear frequently. We show that this variability can be attributed to the presence of a large number of metastable mobile genetic elements on its chromosome. In fact, the genome sequence of <it>B. petrii </it>revealed the presence of at least seven large genomic islands mostly encoding accessory metabolic functions involved in the degradation of aromatic compounds and detoxification of heavy metals. Four of these islands (termed GI1 to GI3 and GI6) are highly related to ICE<it>clc </it>of <it>Pseudomonas knackmussii </it>sp. strain B13. Here we present first data about the molecular characterization of these islands. We defined the exact borders of each island and we show that during standard culture of the bacteria these islands get excised from the chromosome. For all but one of these islands (GI5) we could detect circular intermediates. For the <it>clc</it>-like elements GI1 to GI3 of <it>B. petrii </it>we provide evidence that tandem insertion of these islands which all encode highly related integrases and attachment sites may also lead to incorporation of genomic DNA which originally was not part of the island and to the formation of huge composite islands. By integration of a tetracycline resistance cassette into GI3 we found this island to be rather unstable and to be lost from the bacterial population within about 100 consecutive generations. Furthermore, we show that GI3 is self transmissible and by conjugation can be transferred to <it>B. bronchiseptica </it>thus proving it to be an active integrative and conjugative element</p> <p>Conclusion</p> <p>The results show that phenotypic variation of <it>B. petrii </it>is correlated with the presence of genomic islands. Tandem integration of related islands may contribute to island evolution by the acquisition of genes originally belonging to the bacterial core genome. In conclusion, <it>B. petrii </it>appears to be the first member of the genus in which horizontal gene transfer events have massively shaped its genome structure.</p>http://www.biomedcentral.com/1471-2180/9/141
spellingShingle Levillain Erwan
Hubans Christine
Hot David
Bauer Susanne
Schmitt Karin
Lechner Melanie
Locht Camille
Lemoine Yves
Gross Roy
Genomic island excisions in <it>Bordetella petrii</it>
BMC Microbiology
title Genomic island excisions in <it>Bordetella petrii</it>
title_full Genomic island excisions in <it>Bordetella petrii</it>
title_fullStr Genomic island excisions in <it>Bordetella petrii</it>
title_full_unstemmed Genomic island excisions in <it>Bordetella petrii</it>
title_short Genomic island excisions in <it>Bordetella petrii</it>
title_sort genomic island excisions in it bordetella petrii it
url http://www.biomedcentral.com/1471-2180/9/141
work_keys_str_mv AT levillainerwan genomicislandexcisionsinitbordetellapetriiit
AT hubanschristine genomicislandexcisionsinitbordetellapetriiit
AT hotdavid genomicislandexcisionsinitbordetellapetriiit
AT bauersusanne genomicislandexcisionsinitbordetellapetriiit
AT schmittkarin genomicislandexcisionsinitbordetellapetriiit
AT lechnermelanie genomicislandexcisionsinitbordetellapetriiit
AT lochtcamille genomicislandexcisionsinitbordetellapetriiit
AT lemoineyves genomicislandexcisionsinitbordetellapetriiit
AT grossroy genomicislandexcisionsinitbordetellapetriiit