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A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies
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| Zeitschriftentitel: | mBio |
|---|---|
| Personen und Körperschaften: | , , |
| In: | mBio, 8, 2017, 4 |
| Format: | E-Article |
| Sprache: | Englisch |
| veröffentlicht: |
American Society for Microbiology
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| Schlagwörter: |
| author_facet |
Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora |
|---|---|
| author |
Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora |
| spellingShingle |
Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora mBio A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies Virology Microbiology |
| author_sort |
lazzaro, martina |
| spelling |
Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora 2161-2129 2150-7511 American Society for Microbiology Virology Microbiology http://dx.doi.org/10.1128/mbio.00559-17 <jats:title>ABSTRACT</jats:title> <jats:p> The ability to detect and measure danger from an environmental signal is paramount for bacteria to respond accordingly, deploying strategies that halt or counteract potential cellular injury and maximize survival chances. Type VI secretion systems (T6SSs) are complex bacterial contractile nanomachines able to target toxic effectors into neighboring bacteria competing for the same colonization niche. Previous studies support the concept that either T6SSs are constitutively active or they fire effectors in response to various stimuli, such as high bacterial density, cell-cell contact, nutrient depletion, or components from dead sibling cells. For <jats:italic>Serratia marcescens</jats:italic> , it has been proposed that its T6SS is stochastically expressed, with no distinction between harmless or aggressive competitors. In contrast, we demonstrate that the Rcs regulatory system is responsible for finely tuning <jats:italic>Serratia</jats:italic> T6SS expression levels, behaving as a transcriptional rheostat. When confronted with harmless bacteria, basal T6SS expression levels suffice for <jats:italic>Serratia</jats:italic> to eliminate the competitor. A moderate T6SS upregulation is triggered when, according to the aggressor-prey ratio, an unbalanced interplay between homologous and heterologous effectors and immunity proteins takes place. Higher T6SS expression levels are achieved when <jats:italic>Serratia</jats:italic> is challenged by a contender like <jats:italic>Acinetobacter</jats:italic> , which indiscriminately fires heterologous effectors able to exert lethal cellular harm, threatening the survival of the <jats:italic>Serratia</jats:italic> population. We also demonstrate that <jats:italic>Serratia</jats:italic> ’s RcsB-dependent T6SS regulatory mechanism responds not to general stress signals but to the action of specific effectors from competitors, displaying an exquisite strategy to weigh risks and keep the balance between energy expenditure and fitness costs. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> <jats:italic>Serratia marcescens</jats:italic> is among the health-threatening pathogens categorized by the WHO as research priorities to develop alternative antimicrobial strategies, and it was also recently identified as one major component of the gut microbiome in familial Crohn disease dysbiosis. Type VI secretion systems (T6SSs) stand among the array of survival strategies that <jats:italic>Serratia</jats:italic> displays. They are contractile multiprotein complexes able to deliver toxic effectors directed to kill bacterial species sharing the same niche and, thus, competing for vital resources. Here, we show that <jats:italic>Serratia</jats:italic> is able to detect and measure the extent of damage generated through T6SS-delivered toxins from neighboring bacteria and responds by transcriptionally adjusting the expression level of its own T6SS machinery to counterattack the rival. This strategy allows <jats:italic>Serratia</jats:italic> to finely tune the production of costly T6SS devices to maximize the chances of successfully fighting against enemies and minimize energy investment. The knowledge of this novel mechanism provides insight to better understand bacterial interactions and design alternative treatments for polymicrobial infections. </jats:p> A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies mBio |
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10.1128/mbio.00559-17 |
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Biologie Medizin |
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American Society for Microbiology, 2017 |
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American Society for Microbiology, 2017 |
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2161-2129 2150-7511 |
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2017 |
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American Society for Microbiology |
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mBio |
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49 |
| title |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_unstemmed |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_full |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_fullStr |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_full_unstemmed |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_short |
A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_sort |
a transcriptional regulatory mechanism finely tunes the firing of type vi secretion system in response to bacterial enemies |
| topic |
Virology Microbiology |
| url |
http://dx.doi.org/10.1128/mbio.00559-17 |
| publishDate |
2017 |
| physical |
|
| description |
<jats:title>ABSTRACT</jats:title>
<jats:p>
The ability to detect and measure danger from an environmental signal is paramount for bacteria to respond accordingly, deploying strategies that halt or counteract potential cellular injury and maximize survival chances. Type VI secretion systems (T6SSs) are complex bacterial contractile nanomachines able to target toxic effectors into neighboring bacteria competing for the same colonization niche. Previous studies support the concept that either T6SSs are constitutively active or they fire effectors in response to various stimuli, such as high bacterial density, cell-cell contact, nutrient depletion, or components from dead sibling cells. For
<jats:italic>Serratia marcescens</jats:italic>
, it has been proposed that its T6SS is stochastically expressed, with no distinction between harmless or aggressive competitors. In contrast, we demonstrate that the Rcs regulatory system is responsible for finely tuning
<jats:italic>Serratia</jats:italic>
T6SS expression levels, behaving as a transcriptional rheostat. When confronted with harmless bacteria, basal T6SS expression levels suffice for
<jats:italic>Serratia</jats:italic>
to eliminate the competitor. A moderate T6SS upregulation is triggered when, according to the aggressor-prey ratio, an unbalanced interplay between homologous and heterologous effectors and immunity proteins takes place. Higher T6SS expression levels are achieved when
<jats:italic>Serratia</jats:italic>
is challenged by a contender like
<jats:italic>Acinetobacter</jats:italic>
, which indiscriminately fires heterologous effectors able to exert lethal cellular harm, threatening the survival of the
<jats:italic>Serratia</jats:italic>
population. We also demonstrate that
<jats:italic>Serratia</jats:italic>
’s RcsB-dependent T6SS regulatory mechanism responds not to general stress signals but to the action of specific effectors from competitors, displaying an exquisite strategy to weigh risks and keep the balance between energy expenditure and fitness costs.
</jats:p>
<jats:p>
<jats:bold>IMPORTANCE</jats:bold>
<jats:italic>Serratia marcescens</jats:italic>
is among the health-threatening pathogens categorized by the WHO as research priorities to develop alternative antimicrobial strategies, and it was also recently identified as one major component of the gut microbiome in familial Crohn disease dysbiosis. Type VI secretion systems (T6SSs) stand among the array of survival strategies that
<jats:italic>Serratia</jats:italic>
displays. They are contractile multiprotein complexes able to deliver toxic effectors directed to kill bacterial species sharing the same niche and, thus, competing for vital resources. Here, we show that
<jats:italic>Serratia</jats:italic>
is able to detect and measure the extent of damage generated through T6SS-delivered toxins from neighboring bacteria and responds by transcriptionally adjusting the expression level of its own T6SS machinery to counterattack the rival. This strategy allows
<jats:italic>Serratia</jats:italic>
to finely tune the production of costly T6SS devices to maximize the chances of successfully fighting against enemies and minimize energy investment. The knowledge of this novel mechanism provides insight to better understand bacterial interactions and design alternative treatments for polymicrobial infections.
</jats:p> |
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| author | Lazzaro, Martina, Feldman, Mario F., García Véscovi, Eleonora |
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| description | <jats:title>ABSTRACT</jats:title> <jats:p> The ability to detect and measure danger from an environmental signal is paramount for bacteria to respond accordingly, deploying strategies that halt or counteract potential cellular injury and maximize survival chances. Type VI secretion systems (T6SSs) are complex bacterial contractile nanomachines able to target toxic effectors into neighboring bacteria competing for the same colonization niche. Previous studies support the concept that either T6SSs are constitutively active or they fire effectors in response to various stimuli, such as high bacterial density, cell-cell contact, nutrient depletion, or components from dead sibling cells. For <jats:italic>Serratia marcescens</jats:italic> , it has been proposed that its T6SS is stochastically expressed, with no distinction between harmless or aggressive competitors. In contrast, we demonstrate that the Rcs regulatory system is responsible for finely tuning <jats:italic>Serratia</jats:italic> T6SS expression levels, behaving as a transcriptional rheostat. When confronted with harmless bacteria, basal T6SS expression levels suffice for <jats:italic>Serratia</jats:italic> to eliminate the competitor. A moderate T6SS upregulation is triggered when, according to the aggressor-prey ratio, an unbalanced interplay between homologous and heterologous effectors and immunity proteins takes place. Higher T6SS expression levels are achieved when <jats:italic>Serratia</jats:italic> is challenged by a contender like <jats:italic>Acinetobacter</jats:italic> , which indiscriminately fires heterologous effectors able to exert lethal cellular harm, threatening the survival of the <jats:italic>Serratia</jats:italic> population. We also demonstrate that <jats:italic>Serratia</jats:italic> ’s RcsB-dependent T6SS regulatory mechanism responds not to general stress signals but to the action of specific effectors from competitors, displaying an exquisite strategy to weigh risks and keep the balance between energy expenditure and fitness costs. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> <jats:italic>Serratia marcescens</jats:italic> is among the health-threatening pathogens categorized by the WHO as research priorities to develop alternative antimicrobial strategies, and it was also recently identified as one major component of the gut microbiome in familial Crohn disease dysbiosis. Type VI secretion systems (T6SSs) stand among the array of survival strategies that <jats:italic>Serratia</jats:italic> displays. They are contractile multiprotein complexes able to deliver toxic effectors directed to kill bacterial species sharing the same niche and, thus, competing for vital resources. Here, we show that <jats:italic>Serratia</jats:italic> is able to detect and measure the extent of damage generated through T6SS-delivered toxins from neighboring bacteria and responds by transcriptionally adjusting the expression level of its own T6SS machinery to counterattack the rival. This strategy allows <jats:italic>Serratia</jats:italic> to finely tune the production of costly T6SS devices to maximize the chances of successfully fighting against enemies and minimize energy investment. The knowledge of this novel mechanism provides insight to better understand bacterial interactions and design alternative treatments for polymicrobial infections. </jats:p> |
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| spelling | Lazzaro, Martina Feldman, Mario F. García Véscovi, Eleonora 2161-2129 2150-7511 American Society for Microbiology Virology Microbiology http://dx.doi.org/10.1128/mbio.00559-17 <jats:title>ABSTRACT</jats:title> <jats:p> The ability to detect and measure danger from an environmental signal is paramount for bacteria to respond accordingly, deploying strategies that halt or counteract potential cellular injury and maximize survival chances. Type VI secretion systems (T6SSs) are complex bacterial contractile nanomachines able to target toxic effectors into neighboring bacteria competing for the same colonization niche. Previous studies support the concept that either T6SSs are constitutively active or they fire effectors in response to various stimuli, such as high bacterial density, cell-cell contact, nutrient depletion, or components from dead sibling cells. For <jats:italic>Serratia marcescens</jats:italic> , it has been proposed that its T6SS is stochastically expressed, with no distinction between harmless or aggressive competitors. In contrast, we demonstrate that the Rcs regulatory system is responsible for finely tuning <jats:italic>Serratia</jats:italic> T6SS expression levels, behaving as a transcriptional rheostat. When confronted with harmless bacteria, basal T6SS expression levels suffice for <jats:italic>Serratia</jats:italic> to eliminate the competitor. A moderate T6SS upregulation is triggered when, according to the aggressor-prey ratio, an unbalanced interplay between homologous and heterologous effectors and immunity proteins takes place. Higher T6SS expression levels are achieved when <jats:italic>Serratia</jats:italic> is challenged by a contender like <jats:italic>Acinetobacter</jats:italic> , which indiscriminately fires heterologous effectors able to exert lethal cellular harm, threatening the survival of the <jats:italic>Serratia</jats:italic> population. We also demonstrate that <jats:italic>Serratia</jats:italic> ’s RcsB-dependent T6SS regulatory mechanism responds not to general stress signals but to the action of specific effectors from competitors, displaying an exquisite strategy to weigh risks and keep the balance between energy expenditure and fitness costs. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> <jats:italic>Serratia marcescens</jats:italic> is among the health-threatening pathogens categorized by the WHO as research priorities to develop alternative antimicrobial strategies, and it was also recently identified as one major component of the gut microbiome in familial Crohn disease dysbiosis. Type VI secretion systems (T6SSs) stand among the array of survival strategies that <jats:italic>Serratia</jats:italic> displays. They are contractile multiprotein complexes able to deliver toxic effectors directed to kill bacterial species sharing the same niche and, thus, competing for vital resources. Here, we show that <jats:italic>Serratia</jats:italic> is able to detect and measure the extent of damage generated through T6SS-delivered toxins from neighboring bacteria and responds by transcriptionally adjusting the expression level of its own T6SS machinery to counterattack the rival. This strategy allows <jats:italic>Serratia</jats:italic> to finely tune the production of costly T6SS devices to maximize the chances of successfully fighting against enemies and minimize energy investment. The knowledge of this novel mechanism provides insight to better understand bacterial interactions and design alternative treatments for polymicrobial infections. </jats:p> A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies mBio |
| spellingShingle | Lazzaro, Martina, Feldman, Mario F., García Véscovi, Eleonora, mBio, A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies, Virology, Microbiology |
| title | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_full | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_fullStr | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_full_unstemmed | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_short | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| title_sort | a transcriptional regulatory mechanism finely tunes the firing of type vi secretion system in response to bacterial enemies |
| title_unstemmed | A Transcriptional Regulatory Mechanism Finely Tunes the Firing of Type VI Secretion System in Response to Bacterial Enemies |
| topic | Virology, Microbiology |
| url | http://dx.doi.org/10.1128/mbio.00559-17 |