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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2016-05-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00240-16 |
| _version_ | 1819038276346970112 |
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| author | Thomas P. Burke Daniel A. Portnoy |
| author_facet | Thomas P. Burke Daniel A. Portnoy |
| author_sort | Thomas P. Burke |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-21T08:34:44Z |
| format | Article |
| id | doaj.art-0d0cd57f43ec4e67ba908630cd25e57b |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-21T08:34:44Z |
| publishDate | 2016-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-0d0cd57f43ec4e67ba908630cd25e57b2022-12-21T19:10:06ZengAmerican Society for MicrobiologymBio2150-75112016-05-017210.1128/mBio.00240-16SpoVG Is a Conserved RNA-Binding Protein That Regulates <named-content content-type="genus-species">Listeria monocytogenes</named-content> Lysozyme Resistance, Virulence, and Swarming MotilityThomas P. Burke0Daniel A. Portnoy1Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, USADepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.00240-16 |
| spellingShingle | 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 mBio |
| 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_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_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_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 |
| url | https://journals.asm.org/doi/10.1128/mBio.00240-16 |
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