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The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development
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| Zeitschriftentitel: | Journal of Bacteriology |
|---|---|
| Personen und Körperschaften: | , |
| In: | Journal of Bacteriology, 199, 2017, 10 |
| Format: | E-Article |
| Sprache: | Englisch |
| veröffentlicht: |
American Society for Microbiology
|
| Schlagwörter: |
| author_facet |
Rajagopalan, Ramya Kroos, Lee Rajagopalan, Ramya Kroos, Lee |
|---|---|
| author |
Rajagopalan, Ramya Kroos, Lee |
| spellingShingle |
Rajagopalan, Ramya Kroos, Lee Journal of Bacteriology The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development Molecular Biology Microbiology |
| author_sort |
rajagopalan, ramya |
| spelling |
Rajagopalan, Ramya Kroos, Lee 0021-9193 1098-5530 American Society for Microbiology Molecular Biology Microbiology http://dx.doi.org/10.1128/jb.00788-16 <jats:title>ABSTRACT</jats:title> <jats:p> <jats:named-content content-type="genus-species">Myxococcus xanthus</jats:named-content> undergoes multicellular development when starved. Thousands of rod-shaped cells coordinate their movements and aggregate into mounds in which cells differentiate into spores. Mutations in the <jats:italic>dev</jats:italic> operon impair development. The <jats:italic>dev</jats:italic> operon encompasses a clustered regularly interspaced short palindromic repeat-associated (CRISPR-Cas) system. Null mutations in <jats:italic>devI</jats:italic> , a small gene at the beginning of the <jats:italic>dev</jats:italic> operon, suppress the developmental defects caused by null mutations in the downstream <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> genes but failed to suppress defects caused by a small in-frame deletion in <jats:italic>devT</jats:italic> . We provide evidence that the original mutant has a second-site mutation. We show that <jats:italic>devT</jats:italic> null mutants exhibit developmental defects indistinguishable from <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> null mutants, and a null mutation in <jats:italic>devI</jats:italic> suppresses the defects of a <jats:italic>devT</jats:italic> null mutation. The similarity of DevTRS proteins to components of the CRISPR-associated complex for antiviral defense (Cascade), together with our molecular characterization of <jats:italic>dev</jats:italic> mutants, support a model in which DevTRS form a Cascade-like subcomplex that negatively autoregulates <jats:italic>dev</jats:italic> transcript accumulation and prevents DevI overproduction that would strongly inhibit sporulation. Our results also suggest that DevI transiently inhibits sporulation when regulated normally. The mechanism of transient inhibition may involve MrpC, a key transcription factor, whose translation appears to be weakly inhibited by DevI. Finally, our characterization of a <jats:italic>devI devS</jats:italic> mutant indicates that very little <jats:italic>exo</jats:italic> transcript is required for sporulation, which is surprising since Exo proteins help form the polysaccharide spore coat. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> CRISPR-Cas systems typically function as adaptive immune systems in bacteria. The <jats:italic>dev</jats:italic> CRISPR-Cas system of <jats:named-content content-type="genus-species">M. xanthus</jats:named-content> has been proposed to prevent bacteriophage infection during development, but how <jats:italic>dev</jats:italic> controls sporulation has been elusive. Recent evidence supported a model in which DevR and DevS prevent overproduction of DevI, a predicted 40-residue inhibitor of sporulation. We provide genetic evidence that DevT functions together with DevR and DevS to prevent DevI overproduction. We also show that spores form about 6 h earlier in mutants lacking <jats:italic>devI</jats:italic> than in the wild type. Only a minority of natural isolates appear to have a functional <jats:italic>dev</jats:italic> promoter and <jats:italic>devI</jats:italic> , suggesting that a functional <jats:italic>dev</jats:italic> CRISPR-Cas system evolved recently in niches where delayed sporulation and/or protection from bacteriophage infection proved advantageous. </jats:p> The <i>dev</i> Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development Journal of Bacteriology |
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10.1128/jb.00788-16 |
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Online Free |
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Biologie |
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American Society for Microbiology, 2017 |
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American Society for Microbiology, 2017 |
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0021-9193 1098-5530 |
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0021-9193 1098-5530 |
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rajagopalan2017thedevoperonregulatesthetimingofsporulationduringmyxococcusxanthusdevelopment |
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2017 |
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American Society for Microbiology |
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ai |
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ai |
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Journal of Bacteriology |
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49 |
| title |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_unstemmed |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_full |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_fullStr |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_full_unstemmed |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_short |
The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_sort |
the
<i>dev</i>
operon regulates the timing of sporulation during myxococcus xanthus development |
| topic |
Molecular Biology Microbiology |
| url |
http://dx.doi.org/10.1128/jb.00788-16 |
| publishDate |
2017 |
| physical |
|
| description |
<jats:title>ABSTRACT</jats:title>
<jats:p>
<jats:named-content content-type="genus-species">Myxococcus xanthus</jats:named-content>
undergoes multicellular development when starved. Thousands of rod-shaped cells coordinate their movements and aggregate into mounds in which cells differentiate into spores. Mutations in the
<jats:italic>dev</jats:italic>
operon impair development. The
<jats:italic>dev</jats:italic>
operon encompasses a clustered regularly interspaced short palindromic repeat-associated (CRISPR-Cas) system. Null mutations in
<jats:italic>devI</jats:italic>
, a small gene at the beginning of the
<jats:italic>dev</jats:italic>
operon, suppress the developmental defects caused by null mutations in the downstream
<jats:italic>devR</jats:italic>
and
<jats:italic>devS</jats:italic>
genes but failed to suppress defects caused by a small in-frame deletion in
<jats:italic>devT</jats:italic>
. We provide evidence that the original mutant has a second-site mutation. We show that
<jats:italic>devT</jats:italic>
null mutants exhibit developmental defects indistinguishable from
<jats:italic>devR</jats:italic>
and
<jats:italic>devS</jats:italic>
null mutants, and a null mutation in
<jats:italic>devI</jats:italic>
suppresses the defects of a
<jats:italic>devT</jats:italic>
null mutation. The similarity of DevTRS proteins to components of the CRISPR-associated complex for antiviral defense (Cascade), together with our molecular characterization of
<jats:italic>dev</jats:italic>
mutants, support a model in which DevTRS form a Cascade-like subcomplex that negatively autoregulates
<jats:italic>dev</jats:italic>
transcript accumulation and prevents DevI overproduction that would strongly inhibit sporulation. Our results also suggest that DevI transiently inhibits sporulation when regulated normally. The mechanism of transient inhibition may involve MrpC, a key transcription factor, whose translation appears to be weakly inhibited by DevI. Finally, our characterization of a
<jats:italic>devI devS</jats:italic>
mutant indicates that very little
<jats:italic>exo</jats:italic>
transcript is required for sporulation, which is surprising since Exo proteins help form the polysaccharide spore coat.
</jats:p>
<jats:p>
<jats:bold>IMPORTANCE</jats:bold>
CRISPR-Cas systems typically function as adaptive immune systems in bacteria. The
<jats:italic>dev</jats:italic>
CRISPR-Cas system of
<jats:named-content content-type="genus-species">M. xanthus</jats:named-content>
has been proposed to prevent bacteriophage infection during development, but how
<jats:italic>dev</jats:italic>
controls sporulation has been elusive. Recent evidence supported a model in which DevR and DevS prevent overproduction of DevI, a predicted 40-residue inhibitor of sporulation. We provide genetic evidence that DevT functions together with DevR and DevS to prevent DevI overproduction. We also show that spores form about 6 h earlier in mutants lacking
<jats:italic>devI</jats:italic>
than in the wild type. Only a minority of natural isolates appear to have a functional
<jats:italic>dev</jats:italic>
promoter and
<jats:italic>devI</jats:italic>
, suggesting that a functional
<jats:italic>dev</jats:italic>
CRISPR-Cas system evolved recently in niches where delayed sporulation and/or protection from bacteriophage infection proved advantageous.
</jats:p> |
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| author | Rajagopalan, Ramya, Kroos, Lee |
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| description | <jats:title>ABSTRACT</jats:title> <jats:p> <jats:named-content content-type="genus-species">Myxococcus xanthus</jats:named-content> undergoes multicellular development when starved. Thousands of rod-shaped cells coordinate their movements and aggregate into mounds in which cells differentiate into spores. Mutations in the <jats:italic>dev</jats:italic> operon impair development. The <jats:italic>dev</jats:italic> operon encompasses a clustered regularly interspaced short palindromic repeat-associated (CRISPR-Cas) system. Null mutations in <jats:italic>devI</jats:italic> , a small gene at the beginning of the <jats:italic>dev</jats:italic> operon, suppress the developmental defects caused by null mutations in the downstream <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> genes but failed to suppress defects caused by a small in-frame deletion in <jats:italic>devT</jats:italic> . We provide evidence that the original mutant has a second-site mutation. We show that <jats:italic>devT</jats:italic> null mutants exhibit developmental defects indistinguishable from <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> null mutants, and a null mutation in <jats:italic>devI</jats:italic> suppresses the defects of a <jats:italic>devT</jats:italic> null mutation. The similarity of DevTRS proteins to components of the CRISPR-associated complex for antiviral defense (Cascade), together with our molecular characterization of <jats:italic>dev</jats:italic> mutants, support a model in which DevTRS form a Cascade-like subcomplex that negatively autoregulates <jats:italic>dev</jats:italic> transcript accumulation and prevents DevI overproduction that would strongly inhibit sporulation. Our results also suggest that DevI transiently inhibits sporulation when regulated normally. The mechanism of transient inhibition may involve MrpC, a key transcription factor, whose translation appears to be weakly inhibited by DevI. Finally, our characterization of a <jats:italic>devI devS</jats:italic> mutant indicates that very little <jats:italic>exo</jats:italic> transcript is required for sporulation, which is surprising since Exo proteins help form the polysaccharide spore coat. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> CRISPR-Cas systems typically function as adaptive immune systems in bacteria. The <jats:italic>dev</jats:italic> CRISPR-Cas system of <jats:named-content content-type="genus-species">M. xanthus</jats:named-content> has been proposed to prevent bacteriophage infection during development, but how <jats:italic>dev</jats:italic> controls sporulation has been elusive. Recent evidence supported a model in which DevR and DevS prevent overproduction of DevI, a predicted 40-residue inhibitor of sporulation. We provide genetic evidence that DevT functions together with DevR and DevS to prevent DevI overproduction. We also show that spores form about 6 h earlier in mutants lacking <jats:italic>devI</jats:italic> than in the wild type. Only a minority of natural isolates appear to have a functional <jats:italic>dev</jats:italic> promoter and <jats:italic>devI</jats:italic> , suggesting that a functional <jats:italic>dev</jats:italic> CRISPR-Cas system evolved recently in niches where delayed sporulation and/or protection from bacteriophage infection proved advantageous. </jats:p> |
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| spelling | Rajagopalan, Ramya Kroos, Lee 0021-9193 1098-5530 American Society for Microbiology Molecular Biology Microbiology http://dx.doi.org/10.1128/jb.00788-16 <jats:title>ABSTRACT</jats:title> <jats:p> <jats:named-content content-type="genus-species">Myxococcus xanthus</jats:named-content> undergoes multicellular development when starved. Thousands of rod-shaped cells coordinate their movements and aggregate into mounds in which cells differentiate into spores. Mutations in the <jats:italic>dev</jats:italic> operon impair development. The <jats:italic>dev</jats:italic> operon encompasses a clustered regularly interspaced short palindromic repeat-associated (CRISPR-Cas) system. Null mutations in <jats:italic>devI</jats:italic> , a small gene at the beginning of the <jats:italic>dev</jats:italic> operon, suppress the developmental defects caused by null mutations in the downstream <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> genes but failed to suppress defects caused by a small in-frame deletion in <jats:italic>devT</jats:italic> . We provide evidence that the original mutant has a second-site mutation. We show that <jats:italic>devT</jats:italic> null mutants exhibit developmental defects indistinguishable from <jats:italic>devR</jats:italic> and <jats:italic>devS</jats:italic> null mutants, and a null mutation in <jats:italic>devI</jats:italic> suppresses the defects of a <jats:italic>devT</jats:italic> null mutation. The similarity of DevTRS proteins to components of the CRISPR-associated complex for antiviral defense (Cascade), together with our molecular characterization of <jats:italic>dev</jats:italic> mutants, support a model in which DevTRS form a Cascade-like subcomplex that negatively autoregulates <jats:italic>dev</jats:italic> transcript accumulation and prevents DevI overproduction that would strongly inhibit sporulation. Our results also suggest that DevI transiently inhibits sporulation when regulated normally. The mechanism of transient inhibition may involve MrpC, a key transcription factor, whose translation appears to be weakly inhibited by DevI. Finally, our characterization of a <jats:italic>devI devS</jats:italic> mutant indicates that very little <jats:italic>exo</jats:italic> transcript is required for sporulation, which is surprising since Exo proteins help form the polysaccharide spore coat. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> CRISPR-Cas systems typically function as adaptive immune systems in bacteria. The <jats:italic>dev</jats:italic> CRISPR-Cas system of <jats:named-content content-type="genus-species">M. xanthus</jats:named-content> has been proposed to prevent bacteriophage infection during development, but how <jats:italic>dev</jats:italic> controls sporulation has been elusive. Recent evidence supported a model in which DevR and DevS prevent overproduction of DevI, a predicted 40-residue inhibitor of sporulation. We provide genetic evidence that DevT functions together with DevR and DevS to prevent DevI overproduction. We also show that spores form about 6 h earlier in mutants lacking <jats:italic>devI</jats:italic> than in the wild type. Only a minority of natural isolates appear to have a functional <jats:italic>dev</jats:italic> promoter and <jats:italic>devI</jats:italic> , suggesting that a functional <jats:italic>dev</jats:italic> CRISPR-Cas system evolved recently in niches where delayed sporulation and/or protection from bacteriophage infection proved advantageous. </jats:p> The <i>dev</i> Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development Journal of Bacteriology |
| spellingShingle | Rajagopalan, Ramya, Kroos, Lee, Journal of Bacteriology, The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development, Molecular Biology, Microbiology |
| title | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_full | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_fullStr | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_full_unstemmed | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_short | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| title_sort | the <i>dev</i> operon regulates the timing of sporulation during myxococcus xanthus development |
| title_unstemmed | The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development |
| topic | Molecular Biology, Microbiology |
| url | http://dx.doi.org/10.1128/jb.00788-16 |