Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it>
<p>Abstract</p> <p>Background</p> <p>Two closely related ICEs, ICE<it>St1 </it>and ICE<it>St3</it>, have been identified in the lactic acid bacterium <it>Streptococcus thermophilus</it>. While their conjugation and recombination modul...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2011-10-01
|
| Series: | BMC Microbiology |
| Online Access: | http://www.biomedcentral.com/1471-2180/11/238 |
| _version_ | 1818759112485240832 |
|---|---|
| author | Carraro Nicolas Libante Virginie Morel Catherine Decaris Bernard Charron-Bourgoin Florence Leblond Pierre Guédon Gérard |
| author_facet | Carraro Nicolas Libante Virginie Morel Catherine Decaris Bernard Charron-Bourgoin Florence Leblond Pierre Guédon Gérard |
| author_sort | Carraro Nicolas |
| collection | DOAJ |
| description | <p>Abstract</p> <p>Background</p> <p>Two closely related ICEs, ICE<it>St1 </it>and ICE<it>St3</it>, have been identified in the lactic acid bacterium <it>Streptococcus thermophilus</it>. While their conjugation and recombination modules are almost identical (95% nucleotide identity) and their regulation modules related, previous work has demonstrated that transconjugants carrying ICE<it>St3 </it>were generated at rate exceeding by a 1000 factor that of ICE<it>St1</it>.</p> <p>Results</p> <p>The functional regulation of ICE<it>St1 </it>and ICE<it>St3 </it>transcription, excision and replication were investigated under different conditions (exponential growth or stationary phase, DNA damage by exposition to mitomycin C). Analysis revealed an identical transcriptional organization of their recombination and conjugation modules (long unique transcript) whereas the transcriptional organization of their regulation modules were found to be different (two operons in ICE<it>St1 </it>but only one in ICE<it>St3</it>) and to depend on the conditions (promoter specific of stationary phase in ICE<it>St3</it>). For both elements, stationary phase and DNA damage lead to the rise of transcript levels of the conjugation-recombination and regulation modules. Whatever the growth culture conditions, excision of ICE<it>St1 </it>was found to be lower than that of ICE<it>St3</it>, which is consistent with weaker transfer frequencies. Furthermore, for both elements, excision increases in stationary phase (8.9-fold for ICE<it>St1 </it>and 1.31-fold for ICE<it>St3</it>) and is strongly enhanced by DNA damage (38-fold for ICE<it>St1 </it>and 18-fold for ICE<it>St3</it>). Although ICEs are generally not described as replicative elements, the copy number of ICE<it>St3 </it>exhibited a sharp increase (9.6-fold) after mitomycin C exposure of its harboring strain CNRZ385. This result was not observed when ICE<it>St3 </it>was introduced in a strain deriving ICE<it>St1 </it>host strain CNRZ368, deleted for this element. This finding suggests an impact of the host cell on ICE behavior.</p> <p>Conclusions</p> <p>All together, these results suggest a novel mechanism of regulation shared by ICE<it>St1</it>, ICE<it>St3 </it>and closely related ICEs, which we identified by analysis of recently sequenced genomes of firmicutes. This is the first report of a partial shutdown of the activity of an ICE executed by a strain belonging to its primary host species. The sharp increase of ICE<it>St3 </it>copy number suggests an induction of replication; such conditional intracellular replication may be common among ICEs.</p> |
| first_indexed | 2024-12-18T06:37:33Z |
| format | Article |
| id | doaj.art-32ccfd9c577c468c9ed6748202c5eac5 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-12-18T06:37:33Z |
| publishDate | 2011-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-32ccfd9c577c468c9ed6748202c5eac52022-12-21T21:17:45ZengBMCBMC Microbiology1471-21802011-10-0111123810.1186/1471-2180-11-238Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it>Carraro NicolasLibante VirginieMorel CatherineDecaris BernardCharron-Bourgoin FlorenceLeblond PierreGuédon Gérard<p>Abstract</p> <p>Background</p> <p>Two closely related ICEs, ICE<it>St1 </it>and ICE<it>St3</it>, have been identified in the lactic acid bacterium <it>Streptococcus thermophilus</it>. While their conjugation and recombination modules are almost identical (95% nucleotide identity) and their regulation modules related, previous work has demonstrated that transconjugants carrying ICE<it>St3 </it>were generated at rate exceeding by a 1000 factor that of ICE<it>St1</it>.</p> <p>Results</p> <p>The functional regulation of ICE<it>St1 </it>and ICE<it>St3 </it>transcription, excision and replication were investigated under different conditions (exponential growth or stationary phase, DNA damage by exposition to mitomycin C). Analysis revealed an identical transcriptional organization of their recombination and conjugation modules (long unique transcript) whereas the transcriptional organization of their regulation modules were found to be different (two operons in ICE<it>St1 </it>but only one in ICE<it>St3</it>) and to depend on the conditions (promoter specific of stationary phase in ICE<it>St3</it>). For both elements, stationary phase and DNA damage lead to the rise of transcript levels of the conjugation-recombination and regulation modules. Whatever the growth culture conditions, excision of ICE<it>St1 </it>was found to be lower than that of ICE<it>St3</it>, which is consistent with weaker transfer frequencies. Furthermore, for both elements, excision increases in stationary phase (8.9-fold for ICE<it>St1 </it>and 1.31-fold for ICE<it>St3</it>) and is strongly enhanced by DNA damage (38-fold for ICE<it>St1 </it>and 18-fold for ICE<it>St3</it>). Although ICEs are generally not described as replicative elements, the copy number of ICE<it>St3 </it>exhibited a sharp increase (9.6-fold) after mitomycin C exposure of its harboring strain CNRZ385. This result was not observed when ICE<it>St3 </it>was introduced in a strain deriving ICE<it>St1 </it>host strain CNRZ368, deleted for this element. This finding suggests an impact of the host cell on ICE behavior.</p> <p>Conclusions</p> <p>All together, these results suggest a novel mechanism of regulation shared by ICE<it>St1</it>, ICE<it>St3 </it>and closely related ICEs, which we identified by analysis of recently sequenced genomes of firmicutes. This is the first report of a partial shutdown of the activity of an ICE executed by a strain belonging to its primary host species. The sharp increase of ICE<it>St3 </it>copy number suggests an induction of replication; such conditional intracellular replication may be common among ICEs.</p>http://www.biomedcentral.com/1471-2180/11/238 |
| spellingShingle | Carraro Nicolas Libante Virginie Morel Catherine Decaris Bernard Charron-Bourgoin Florence Leblond Pierre Guédon Gérard Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> BMC Microbiology |
| title | Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> |
| title_full | Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> |
| title_fullStr | Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> |
| title_full_unstemmed | Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> |
| title_short | Differential regulation of two closely related integrative and conjugative elements from <it>Streptococcus thermophilus</it> |
| title_sort | differential regulation of two closely related integrative and conjugative elements from it streptococcus thermophilus it |
| url | http://www.biomedcentral.com/1471-2180/11/238 |
| work_keys_str_mv | AT carraronicolas differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT libantevirginie differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT morelcatherine differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT decarisbernard differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT charronbourgoinflorence differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT leblondpierre differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit AT guedongerard differentialregulationoftwocloselyrelatedintegrativeandconjugativeelementsfromitstreptococcusthermophilusit |