Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis
Summary Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early st...
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Published in | Molecular microbiology Vol. 78; no. 4; pp. 903 - 915 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford, UK
Blackwell Publishing Ltd
01.11.2010
Blackwell |
Subjects | |
Online Access | Get full text |
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Abstract | Summary
Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. |
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AbstractList | Summary
Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host-microbe associations are less well recognized. During the early stages of the squid-vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host-derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal-sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host-derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host-microbe associations are less well recognized. During the early stages of the squid-vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host-derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A ...hmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the ...hmp strain fails to form normal-sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host-derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. (ProQuest: ... denotes formulae/symbols omitted.) SummaryNitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host-microbe associations are less well recognized. During the early stages of the squid-vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host-derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Delta hmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Delta hmp strain fails to form normal-sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host-derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. |
Author | McFall‐Ngai, Margaret J. Wilneff, Jacqueline Spiro, Stephen Dunn, Anne K. Wang, Yanling Ruby, Edward G. |
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Keywords | Symbiosis Cephalopoda Vibrio fischeri Squid Nitric oxide Bacteria Vibrionaceae Invertebrata Mollusca |
Language | English |
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Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and... Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection... SummaryNitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection... |
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SubjectTerms | Aerobiosis Aliivibrio fischeri - immunology Aliivibrio fischeri - physiology Anaerobiosis Animals Bacterial Proteins - metabolism Bacteriology Biological and medical sciences Decapodiformes - immunology Decapodiformes - microbiology Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Profiling Gram-negative bacteria Hemeproteins - metabolism Microbiology Miscellaneous Mutation Nitric oxide Nitric Oxide - metabolism Nitric Oxide - toxicity Oxidative stress Repressor Proteins - metabolism Signal transduction Symbiosis Vibrio fischeri |
Title | Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis |
URI | https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1365-2958.2010.07376.x https://www.ncbi.nlm.nih.gov/pubmed/20815823 https://www.proquest.com/docview/795244193 https://search.proquest.com/docview/851462023 |
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