The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation

ABSTRACTSporulation is an important feature of the clostridial life cycle, facilitating survival of these bacteria in harsh environments, contributing to disease transmission for pathogenic species, and sharing common early steps that are also involved in regulating industrially important solvent pr...

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Main Authors: Iman Mehdizadeh Gohari, Adrianne N. Edwards, Shonna M. McBride, Bruce A. McClane
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.02248-23
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author Iman Mehdizadeh Gohari
Adrianne N. Edwards
Shonna M. McBride
Bruce A. McClane
author_facet Iman Mehdizadeh Gohari
Adrianne N. Edwards
Shonna M. McBride
Bruce A. McClane
author_sort Iman Mehdizadeh Gohari
collection DOAJ
description ABSTRACTSporulation is an important feature of the clostridial life cycle, facilitating survival of these bacteria in harsh environments, contributing to disease transmission for pathogenic species, and sharing common early steps that are also involved in regulating industrially important solvent production by some non-pathogenic species. Initial genomics studies suggested that Clostridia lack the classical phosphorelay that phosphorylates Spo0A and initiates sporulation in Bacillus, leading to the hypothesis that sporulation in Clostridia universally begins when Spo0A is phosphorylated by orphan histidine kinases (OHKs). However, components of the classical Bacillus phosphorelay were recently identified in some Clostridia. Similar Bacillus phosphorelay components have not yet been found in the pathogenic Clostridia or the solventogenic Clostridia of industrial importance. For some of those Clostridia lacking a classical phosphorelay, the involvement of OHKs in sporulation initiation has received support from genetic studies demonstrating the involvement of several apparent OHKs in their sporulation. In addition, several clostridial OHKs directly phosphorylate Spo0A in vitro. Interestingly, there is considerable protein domain diversity among the sporulation-associated OHKs in Clostridia. Further adding to the emergent complexity of sporulation initiation in Clostridia, several candidate OHK phosphotransfer proteins that were OHK candidates were shown to function as phosphatases that reduce sporulation in some Clostridia. The mounting evidence indicates that no single pathway explains sporulation initiation in all Clostridia and supports the need for further study to fully understand the unexpected and biologically fascinating mechanistic diversity of this important process among these medically and industrially important bacteria.
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spelling doaj.art-f6775f9742c9444da88ea5260b3adcd22024-04-10T13:01:15ZengAmerican Society for MicrobiologymBio2150-75112024-04-0115410.1128/mbio.02248-23The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiationIman Mehdizadeh Gohari0Adrianne N. Edwards1Shonna M. McBride2Bruce A. McClane3Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USADepartment of Microbiology and Immunology, Emory University School of Medicine, Emory Antibiotic Resistance Center, Atlanta, Georgia, USADepartment of Microbiology and Immunology, Emory University School of Medicine, Emory Antibiotic Resistance Center, Atlanta, Georgia, USADepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USAABSTRACTSporulation is an important feature of the clostridial life cycle, facilitating survival of these bacteria in harsh environments, contributing to disease transmission for pathogenic species, and sharing common early steps that are also involved in regulating industrially important solvent production by some non-pathogenic species. Initial genomics studies suggested that Clostridia lack the classical phosphorelay that phosphorylates Spo0A and initiates sporulation in Bacillus, leading to the hypothesis that sporulation in Clostridia universally begins when Spo0A is phosphorylated by orphan histidine kinases (OHKs). However, components of the classical Bacillus phosphorelay were recently identified in some Clostridia. Similar Bacillus phosphorelay components have not yet been found in the pathogenic Clostridia or the solventogenic Clostridia of industrial importance. For some of those Clostridia lacking a classical phosphorelay, the involvement of OHKs in sporulation initiation has received support from genetic studies demonstrating the involvement of several apparent OHKs in their sporulation. In addition, several clostridial OHKs directly phosphorylate Spo0A in vitro. Interestingly, there is considerable protein domain diversity among the sporulation-associated OHKs in Clostridia. Further adding to the emergent complexity of sporulation initiation in Clostridia, several candidate OHK phosphotransfer proteins that were OHK candidates were shown to function as phosphatases that reduce sporulation in some Clostridia. The mounting evidence indicates that no single pathway explains sporulation initiation in all Clostridia and supports the need for further study to fully understand the unexpected and biologically fascinating mechanistic diversity of this important process among these medically and industrially important bacteria.https://journals.asm.org/doi/10.1128/mbio.02248-23ClostridiaSpo0Asporulationhistidine kinasesphosphatases
spellingShingle Iman Mehdizadeh Gohari
Adrianne N. Edwards
Shonna M. McBride
Bruce A. McClane
The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
mBio
Clostridia
Spo0A
sporulation
histidine kinases
phosphatases
title The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
title_full The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
title_fullStr The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
title_full_unstemmed The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
title_short The impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
title_sort impact of orphan histidine kinases and phosphotransfer proteins on the regulation of clostridial sporulation initiation
topic Clostridia
Spo0A
sporulation
histidine kinases
phosphatases
url https://journals.asm.org/doi/10.1128/mbio.02248-23
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