Characterization of Late Acyltransferase Genes of Yersinia pestis and Their Role in Temperature-Dependent Lipid A Variation

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Published inJournal of Bacteriology Vol. 188; no. 4; pp. 1381 - 1388
Main Authors REBEIL, Roberto, ERNST, Robert K, JARRETT, Clayton O, ADAMS, Kristin N, MILLER, Samuel I, HINNEBUSCH, B. Joseph
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.02.2006
Subjects
Acyltransferases - genetics
Acyltransferases - metabolism
Animals
Anti-Bacterial Agents - pharmacology
Anti-Infective Agents - pharmacology
Antimicrobial Cationic Peptides - pharmacology
Bacteriology
Biological and medical sciences
Female
Fundamental and applied biological sciences. Psychology
Gastrointestinal Tract - microbiology
Gene expression
Gene Expression Regulation, Bacterial
Genes, Bacterial - genetics
Insects
Lipid A - chemistry
Lipid A - metabolism
Lipids
Male
Microbial Sensitivity Tests
Microbiology
Miscellaneous
Molecular Biology of Pathogens
Mutation
Pathogens
Polymyxin B - pharmacology
Rodents
Siphonaptera - microbiology
Temperature
Up-Regulation
Yersinia pestis
Yersinia pestis - drug effects
Yersinia pestis - genetics
Yersinia pestis - growth & development
Yersinia pestis - metabolism
Acyltransferases
Temperature
Gene
Microbiology
Enzyme
Transferases
Bacteria
Bacteriology
Enterobacteriaceae
Yersinia pestis
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Abstract Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue JB About JB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0021-9193 Online ISSN: 1098-5530 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JB .asm.org, visit: JB       
AbstractList Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis senses host-specific environmental cues such as temperature and regulates gene expression appropriately to adapt to the insect or mammalian host. For example, Y. pestis synthesizes different forms of lipid A when grown at temperatures corresponding to the in vivo environments of the mammalian host and the flea vector. At 37°C, tetra-acylated lipid A is the major form; but at 26°C or below, hexa-acylated lipid A predominates. In this study, we show that the Y. pestis msbB ( lpxM ) and lpxP homologs encode the acyltransferases that add C 12 and C 16:1 groups, respectively, to lipid IV A to generate the hexa-acylated form, and that their expression is upregulated at 21°C in vitro and in the flea midgut. A Y. pestis ΔmsbB ΔlpxP double mutant that did not produce hexa-acylated lipid A was more sensitive to cecropin A, but not to polymyxin B. This mutant was able to infect and block fleas as well as the parental wild-type strain, indicating that the low-temperature-dependent change to hexa-acylated lipid A synthesis is not required for survival in the flea gut.
Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis senses host-specific environmental cues such as temperature and regulates gene expression appropriately to adapt to the insect or mammalian host. For example, Y. pestis synthesizes different forms of lipid A when grown at temperatures corresponding to the in vivo environments of the mammalian host and the flea vector. At 37 degree C, tetra-acylated lipid A is the major form; but at 26 degree C or below, hexa-acylated lipid A predominates. In this study, we show that the Y. pestis msbB (lpxM) and lpxP homologs encode the acyltransferases that add C sub(12) and C sub(16:1) groups, respectively, to lipid IV sub(A) to generate the hexa-acylated form, and that their expression is upregulated at 21 degree C in vitro and in the flea midgut. A Y. pestis Delta msbB Delta lpxP double mutant that did not produce hexa-acylated lipid A was more sensitive to cecropin A, but not to polymyxin B. This mutant was able to infect and block fleas as well as the parental wild-type strain, indicating that the low-temperature-dependent change to hexa-acylated lipid A synthesis is not required for survival in the flea gut.
ABSTRACT Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis senses host-specific environmental cues such as temperature and regulates gene expression appropriately to adapt to the insect or mammalian host. For example, Y. pestis synthesizes different forms of lipid A when grown at temperatures corresponding to the in vivo environments of the mammalian host and the flea vector. At 37°C, tetra-acylated lipid A is the major form; but at 26°C or below, hexa-acylated lipid A predominates. In this study, we show that the Y. pestis msbB ( lpxM ) and lpxP homologs encode the acyltransferases that add C 12 and C 16:1 groups, respectively, to lipid IV A to generate the hexa-acylated form, and that their expression is upregulated at 21°C in vitro and in the flea midgut. A Y. pestis ΔmsbB ΔlpxP double mutant that did not produce hexa-acylated lipid A was more sensitive to cecropin A, but not to polymyxin B. This mutant was able to infect and block fleas as well as the parental wild-type strain, indicating that the low-temperature-dependent change to hexa-acylated lipid A synthesis is not required for survival in the flea gut.
Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis senses host-specific environmental cues such as temperature and regulates gene expression appropriately to adapt to the insect or mammalian host. For example, Y. pestis synthesizes different forms of lipid A when grown at temperatures corresponding to the in vivo environments of the mammalian host and the flea vector. At 37 degrees C, tetra-acylated lipid A is the major form; but at 26 degrees C or below, hexa-acylated lipid A predominates. In this study, we show that the Y. pestis msbB (lpxM) and lpxP homologs encode the acyltransferases that add C12 and C(16:1) groups, respectively, to lipid IV(A) to generate the hexa-acylated form, and that their expression is upregulated at 21 degrees C in vitro and in the flea midgut. A Y. pestis deltamsbB deltalpxP double mutant that did not produce hexa-acylated lipid A was more sensitive to cecropin A, but not to polymyxin B. This mutant was able to infect and block fleas as well as the parental wild-type strain, indicating that the low-temperature-dependent change to hexa-acylated lipid A synthesis is not required for survival in the flea gut.
Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis senses host-specific environmental cues such as temperature and regulates gene expression appropriately to adapt to the insect or mammalian host. For example, Y. pestis synthesizes different forms of lipid A when grown at temperatures corresponding to the in vivo environments of the mammalian host and the flea vector. At 37 degrees C, tetra-acylated lipid A is the major form; but at 26 degrees C or below, hexa-acylated lipid A predominates. In this study, we show that the Y. pestis msbB (lpxM) and lpxP homologs encode the acyltransferases that add C12 and C16:1 groups, respectively, to lipid IVA to generate the hexa-acylated form, and that their expression is upregulated at 21 degrees C in vitro and in the flea midgut. A Y. pestis msbB lpxP double mutant that did not produce hexa-acylated lipid A was more sensitive to cecropin A, but not to polymyxin B. This mutant was able to infect and block fleas as well as the parental wild-type strain, indicating that the low-temperature-dependent change to hexa-acylated lipid A synthesis is not required for survival in the flea gut. [PUBLICATION ABSTRACT]
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Author Kristin N. Adams
B. Joseph Hinnebusch
Robert K. Ernst
Clayton O. Jarrett
Roberto Rebeil
Samuel I. Miller
AuthorAffiliation Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, 1 Departments of Medicine, 2 Microbiology, 3 Genome Sciences, University of Washington, Seattle, Washington 98195 4
AuthorAffiliation_xml – name: Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, 1 Departments of Medicine, 2 Microbiology, 3 Genome Sciences, University of Washington, Seattle, Washington 98195 4
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  organization: Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, United States
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  surname: ERNST
  fullname: ERNST, Robert K
  organization: Department of Medicine, University of Washington, Seattle, Washington 98195, United States
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  givenname: Clayton O
  surname: JARRETT
  fullname: JARRETT, Clayton O
  organization: Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, United States
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  surname: ADAMS
  fullname: ADAMS, Kristin N
  organization: Department of Medicine, University of Washington, Seattle, Washington 98195, United States
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  organization: Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, United States
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Issue 4
Keywords Acyltransferases
Temperature
Gene
Microbiology
Enzyme
Transferases
Bacteria
Bacteriology
Enterobacteriaceae
Yersinia pestis
Language English
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Corresponding author. Mailing address: Laboratory of Human Bacterial Pathogenesis, NIH, NIAID, Rocky Mountain Laboratories, 903 S. 4th St., Hamilton, MT 59840. Phone: (406) 363-9260. Fax: (406) 363-9394. E-mail: jhinnebusch@niaid.nih.gov.
Present address: Sandia National Laboratory, Albuquerque, NM.
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Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis...
ABSTRACT Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y....
Yersinia pestis is an important human pathogen that is maintained in flea-rodent enzootic cycles in many parts of the world. During its life cycle, Y. pestis...
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StartPage 1381
SubjectTerms Acyltransferases - genetics
Acyltransferases - metabolism
Animals
Anti-Bacterial Agents - pharmacology
Anti-Infective Agents - pharmacology
Antimicrobial Cationic Peptides - pharmacology
Bacteriology
Biological and medical sciences
Female
Fundamental and applied biological sciences. Psychology
Gastrointestinal Tract - microbiology
Gene expression
Gene Expression Regulation, Bacterial
Genes, Bacterial - genetics
Insects
Lipid A - chemistry
Lipid A - metabolism
Lipids
Male
Microbial Sensitivity Tests
Microbiology
Miscellaneous
Molecular Biology of Pathogens
Mutation
Pathogens
Polymyxin B - pharmacology
Rodents
Siphonaptera - microbiology
Temperature
Up-Regulation
Yersinia pestis
Yersinia pestis - drug effects
Yersinia pestis - genetics
Yersinia pestis - growth & development
Yersinia pestis - metabolism
Title Characterization of Late Acyltransferase Genes of Yersinia pestis and Their Role in Temperature-Dependent Lipid A Variation
URI http://jb.asm.org/content/188/4/1381.abstract
https://www.ncbi.nlm.nih.gov/pubmed/16452420
https://www.proquest.com/docview/227095618
https://search.proquest.com/docview/17477603
https://search.proquest.com/docview/67624069
https://pubmed.ncbi.nlm.nih.gov/PMC1367257
Volume 188
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