SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility

ABSTRACT In this study, we sought to characterize the targets of the abundant Listeria monocytogenes noncoding RNA Rli31, which is required for L. monocytogenes lysozyme resistance and pathogenesis. Whole-genome sequencing of lysozyme-resistant suppressor strains identified loss-of-expression mutati...

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Autores principales:	Thomas P. Burke, Daniel A. Portnoy
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0d0cd57f43ec4e67ba908630cd25e57b
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spelling	oai:doaj.org-article:0d0cd57f43ec4e67ba908630cd25e57b2021-11-15T15:41:41ZSpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility10.1128/mBio.00240-162150-7511https://doaj.org/article/0d0cd57f43ec4e67ba908630cd25e57b2016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00240-16https://doaj.org/toc/2150-7511ABSTRACT In this study, we sought to characterize the targets of the abundant Listeria monocytogenes noncoding RNA Rli31, which is required for L. monocytogenes lysozyme resistance and pathogenesis. Whole-genome sequencing of lysozyme-resistant suppressor strains identified loss-of-expression mutations in the promoter of spoVG, and deletion of spoVG rescued lysozyme sensitivity and attenuation in vivo of the rli31 mutant. SpoVG was demonstrated to be an RNA-binding protein that interacted with Rli31 in vitro. The relationship between Rli31 and SpoVG is multifaceted, as both the spoVG-encoded protein and the spoVG 5′-untranslated region interacted with Rli31. In addition, we observed that spoVG-deficient bacteria were nonmotile in soft agar and suppressor mutations that restored swarming motility were identified in the gene encoding a major RNase in Gram-positive bacteria, RNase J1. Collectively, these findings suggest that SpoVG is similar to global posttranscriptional regulators, a class of RNA-binding proteins that interact with noncoding RNA, regulate genes in concert with RNases, and control pleiotropic aspects of bacterial physiology. IMPORTANCE spoVG is widely conserved among bacteria; however, the function of this gene has remained unclear since its initial characterization in 1977. Mutation of spoVG impacts various phenotypes in Gram-positive bacteria, including methicillin resistance, capsule formation, and enzyme secretion in Staphylococcus aureus and also asymmetric cell division, hemolysin production, and sporulation in Bacillus subtilis. Here, we demonstrate that spoVG mutant strains of Listeria monocytogenes are hyper-lysozyme resistant, hypervirulent, nonmotile, and misregulate genes controlling carbon metabolism. Furthermore, we demonstrate that SpoVG is an RNA-binding protein. These findings suggest that SpoVG has a role in L. monocytogenes, and perhaps in other bacteria, as a global gene regulator. Posttranscriptional gene regulators help bacteria adapt to various environments and coordinate differing aspects of bacterial physiology. SpoVG may help the organism coordinate environmental growth and virulence to survive as a facultative pathogen.Thomas P. BurkeDaniel A. PortnoyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Thomas P. Burke Daniel A. Portnoy SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
description	ABSTRACT In this study, we sought to characterize the targets of the abundant Listeria monocytogenes noncoding RNA Rli31, which is required for L. monocytogenes lysozyme resistance and pathogenesis. Whole-genome sequencing of lysozyme-resistant suppressor strains identified loss-of-expression mutations in the promoter of spoVG, and deletion of spoVG rescued lysozyme sensitivity and attenuation in vivo of the rli31 mutant. SpoVG was demonstrated to be an RNA-binding protein that interacted with Rli31 in vitro. The relationship between Rli31 and SpoVG is multifaceted, as both the spoVG-encoded protein and the spoVG 5′-untranslated region interacted with Rli31. In addition, we observed that spoVG-deficient bacteria were nonmotile in soft agar and suppressor mutations that restored swarming motility were identified in the gene encoding a major RNase in Gram-positive bacteria, RNase J1. Collectively, these findings suggest that SpoVG is similar to global posttranscriptional regulators, a class of RNA-binding proteins that interact with noncoding RNA, regulate genes in concert with RNases, and control pleiotropic aspects of bacterial physiology. IMPORTANCE spoVG is widely conserved among bacteria; however, the function of this gene has remained unclear since its initial characterization in 1977. Mutation of spoVG impacts various phenotypes in Gram-positive bacteria, including methicillin resistance, capsule formation, and enzyme secretion in Staphylococcus aureus and also asymmetric cell division, hemolysin production, and sporulation in Bacillus subtilis. Here, we demonstrate that spoVG mutant strains of Listeria monocytogenes are hyper-lysozyme resistant, hypervirulent, nonmotile, and misregulate genes controlling carbon metabolism. Furthermore, we demonstrate that SpoVG is an RNA-binding protein. These findings suggest that SpoVG has a role in L. monocytogenes, and perhaps in other bacteria, as a global gene regulator. Posttranscriptional gene regulators help bacteria adapt to various environments and coordinate differing aspects of bacterial physiology. SpoVG may help the organism coordinate environmental growth and virulence to survive as a facultative pathogen.
format	article
author	Thomas P. Burke Daniel A. Portnoy
author_facet	Thomas P. Burke Daniel A. Portnoy
author_sort	Thomas P. Burke
title	SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
title_short	SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
title_full	SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
title_fullStr	SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
title_full_unstemmed	SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility
title_sort	spovg is a conserved rna-binding protein that regulates <named-content content-type="genus-species">listeria monocytogenes</named-content> lysozyme resistance, virulence, and swarming motility
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/0d0cd57f43ec4e67ba908630cd25e57b
work_keys_str_mv	AT thomaspburke spovgisaconservedrnabindingproteinthatregulatesnamedcontentcontenttypegenusspecieslisteriamonocytogenesnamedcontentlysozymeresistancevirulenceandswarmingmotility AT danielaportnoy spovgisaconservedrnabindingproteinthatregulatesnamedcontentcontenttypegenusspecieslisteriamonocytogenesnamedcontentlysozymeresistancevirulenceandswarmingmotility
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SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming Motility

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