Deciphering the influence of NaCl on social behaviour of Bacillus subtilis

Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm’s development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact...

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Vydáno v:	Royal Society open science Ročník 11; číslo 9; s. 240822 - 16
Hlavní autoři:	Murugan, Prem Anand, Sahu, Muktesh Kumar, Gupta, Manish Kumar, Sankar, T. Sabari, Chandran, Sivasurender, Matheshwaran, Saravanan
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	England The Royal Society Publishing 01.09.2024 The Royal Society
Témata:	Bacillus subtilis Bacteria biofilm Biofilms Drug resistance flagella Gene expression Morphology Motility NaCl Organismal and Evolutionary Biology Physiology Signal transduction Social behavior Sodium chloride surface motility surfactin Viscoelasticity surfactin NaCl flagella surface motility Bacillus subtilis biofilm
ISSN:	2054-5703, 2054-5703
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Abstract	Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm’s development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of Bacillus subtilis . NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor sigD, suggesting the possible underlying mechanisms. To further support these observations, we have used Δ sigD and Δ srfAC null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in B. subtilis from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies.
AbstractList	Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm’s development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of Bacillus subtilis. NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor sigD, suggesting the possible underlying mechanisms. To further support these observations, we have used ΔsigD and ΔsrfAC null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in B. subtilis from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies. Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm's development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of Bacillus subtilis. NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor sigD, suggesting the possible underlying mechanisms. To further support these observations, we have used ΔsigD and ΔsrfAC null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in B. subtilis from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies.Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm's development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of Bacillus subtilis. NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor sigD, suggesting the possible underlying mechanisms. To further support these observations, we have used ΔsigD and ΔsrfAC null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in B. subtilis from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies. Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm’s development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of Bacillus subtilis . NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor sigD, suggesting the possible underlying mechanisms. To further support these observations, we have used Δ sigD and Δ srfAC null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in B. subtilis from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies. Various environmental signals, such as temperature, pH, nutrient levels, salt content and the presence of other microorganisms, can influence biofilm's development and dynamics. However, the innate mechanisms that govern at the molecular and cellular levels remain elusive. Here, we report the impact of physiologically relevant concentrations of NaCl on biofilm formation and the associated differences in an undomesticated natural isolate of . NaCl exposure and its uptake by bacterial cells induced substantial changes in the architecture of pellicle biofilm and an upsurge in the expansion of biofilm colonies on agar surfaces. We have observed the upregulation of genes involved in motility and the downregulation of genes involved in the biosynthesis of extracellular matrix components through the transcription factor suggesting the possible underlying mechanisms. To further support these observations, we have used Δ Δ null mutants, which showed compromised NaCl-induced effects. Our results indicate that NaCl induces a lifestyle shift in from a sessile biofilm state to an independent unicellular motile state. Overall, we present evidence that NaCl can reprogramme gene expression and alter cellular morphology and the state of cells to adapt to motility, which facilitates the expansion of bacterial colonies.
Author	Sankar, T. Sabari Chandran, Sivasurender Gupta, Manish Kumar Matheshwaran, Saravanan Murugan, Prem Anand Sahu, Muktesh Kumar
Author_xml	– sequence: 1 givenname: Prem Anand orcidid: 0000-0002-6681-773X surname: Murugan fullname: Murugan, Prem Anand organization: Department of Biological Sciences and Bioengineering, Indian Institute of Technology , Kanpur, India – sequence: 2 givenname: Muktesh Kumar surname: Sahu fullname: Sahu, Muktesh Kumar organization: Department of Biological Sciences and Bioengineering, Indian Institute of Technology , Kanpur, India – sequence: 3 givenname: Manish Kumar surname: Gupta fullname: Gupta, Manish Kumar organization: Soft and Biological Matter Laboratory, Department of Physics, Indian Institute of Technology , Kanpur, India – sequence: 4 givenname: T. Sabari surname: Sankar fullname: Sankar, T. Sabari organization: School of Biology, Indian Institute of Science Education and Research , Thiruvananthapuram, India – sequence: 5 givenname: Sivasurender orcidid: 0000-0003-0547-0282 surname: Chandran fullname: Chandran, Sivasurender organization: Soft and Biological Matter Laboratory, Department of Physics, Indian Institute of Technology , Kanpur, India – sequence: 6 givenname: Saravanan orcidid: 0000-0001-6762-9928 surname: Matheshwaran fullname: Matheshwaran, Saravanan organization: Department of Biological Sciences and Bioengineering, Indian Institute of Technology , Kanpur, India, Centre for Environmental Sciences and Engineering, Indian Institute of Technology , Kanpur, India, Mehta Family Centre for Engineering in Medicine, Indian Institute of Technology , Kanpur, India
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Keywords	surfactin NaCl flagella surface motility Bacillus subtilis biofilm
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SubjectTerms	Bacillus subtilis Bacteria biofilm Biofilms Drug resistance flagella Gene expression Morphology Motility NaCl Organismal and Evolutionary Biology Physiology Signal transduction Social behavior Sodium chloride surface motility surfactin Viscoelasticity
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Title	Deciphering the influence of NaCl on social behaviour of Bacillus subtilis
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