Adaptation of Listeria monocytogenes to perturbation of c‐di‐AMP metabolism underpins its role in osmoadaptation and identifies a fosfomycin uptake system

Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH respectively. c‐di‐AMP is essential because it prevents the uncontrolled uptake of osmolytes. Here, we studied the phenotypes of cdaA, pdeA,...

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Published inEnvironmental microbiology Vol. 24; no. 9; pp. 4466 - 4488
Main Authors Wang, Mengyi, Wamp, Sabrina, Gibhardt, Johannes, Holland, Gudrun, Schwedt, Inge, Schmidtke, Kai‐Uwe, Scheibner, Katrin, Halbedel, Sven, Commichau, Fabian M.
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.09.2022
Wiley Subscription Services, Inc
Subjects
AMP
Antibiotics
Bacteria
Defects
Deoxyribonucleic acid
DNA
Fosfomycin
Growth
Homeostasis
Isoleucine
Listeria
Listeria monocytogenes
Metabolism
Mutation
Pathogens
Perturbation
Phenotypes
Suppressor mutant
Transportation systems
Uptake
Online AccessGet full text

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Abstract Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH respectively. c‐di‐AMP is essential because it prevents the uncontrolled uptake of osmolytes. Here, we studied the phenotypes of cdaA, pdeA, pgpH and pdeA pgpH mutants with defects in c‐di‐AMP metabolism and characterized suppressor mutants restoring their growth defects. The characterization of the pdeA pgpH mutant revealed that the bacteria show growth defects in defined medium, a phenotype that is invariably suppressed by mutations in cdaA. The previously reported growth defect of the cdaA mutant in rich medium is suppressed by mutations that osmotically stabilize the c‐di‐AMP‐free strain. We also found that the cdaA mutant has an increased sensitivity against isoleucine. The isoleucine‐dependent growth inhibition of the cdaA mutant is suppressed by codY mutations that likely reduce the DNA‐binding activity of encoded CodY variants. Moreover, the characterization of the cdaA suppressor mutants revealed that the Opp oligopeptide transport system is involved in the uptake of the antibiotic fosfomycin. In conclusion, the suppressor analysis corroborates a key function of c‐di‐AMP in controlling osmolyte homeostasis in L. monocytogenes.
AbstractList Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH respectively. c‐di‐AMP is essential because it prevents the uncontrolled uptake of osmolytes. Here, we studied the phenotypes of cdaA , pdeA , pgpH and pdeA pgpH mutants with defects in c‐di‐AMP metabolism and characterized suppressor mutants restoring their growth defects. The characterization of the pdeA pgpH mutant revealed that the bacteria show growth defects in defined medium, a phenotype that is invariably suppressed by mutations in cdaA . The previously reported growth defect of the cdaA mutant in rich medium is suppressed by mutations that osmotically stabilize the c‐di‐AMP‐free strain. We also found that the cdaA mutant has an increased sensitivity against isoleucine. The isoleucine‐dependent growth inhibition of the cdaA mutant is suppressed by codY mutations that likely reduce the DNA‐binding activity of encoded CodY variants. Moreover, the characterization of the cdaA suppressor mutants revealed that the Opp oligopeptide transport system is involved in the uptake of the antibiotic fosfomycin. In conclusion, the suppressor analysis corroborates a key function of c‐di‐AMP in controlling osmolyte homeostasis in L . monocytogenes .
Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH respectively. c‐di‐AMP is essential because it prevents the uncontrolled uptake of osmolytes. Here, we studied the phenotypes of cdaA, pdeA, pgpH and pdeA pgpH mutants with defects in c‐di‐AMP metabolism and characterized suppressor mutants restoring their growth defects. The characterization of the pdeA pgpH mutant revealed that the bacteria show growth defects in defined medium, a phenotype that is invariably suppressed by mutations in cdaA. The previously reported growth defect of the cdaA mutant in rich medium is suppressed by mutations that osmotically stabilize the c‐di‐AMP‐free strain. We also found that the cdaA mutant has an increased sensitivity against isoleucine. The isoleucine‐dependent growth inhibition of the cdaA mutant is suppressed by codY mutations that likely reduce the DNA‐binding activity of encoded CodY variants. Moreover, the characterization of the cdaA suppressor mutants revealed that the Opp oligopeptide transport system is involved in the uptake of the antibiotic fosfomycin. In conclusion, the suppressor analysis corroborates a key function of c‐di‐AMP in controlling osmolyte homeostasis in L. monocytogenes.
The human pathogen Listeria monocytogenes synthesizes and degrades c-di-AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH respectively. c-di-AMP is essential because it prevents the uncontrolled uptake of osmolytes. Here, we studied the phenotypes of cdaA, pdeA, pgpH and pdeA pgpH mutants with defects in c-di-AMP metabolism and characterized suppressor mutants restoring their growth defects. The characterization of the pdeA pgpH mutant revealed that the bacteria show growth defects in defined medium, a phenotype that is invariably suppressed by mutations in cdaA. The previously reported growth defect of the cdaA mutant in rich medium is suppressed by mutations that osmotically stabilize the c-di-AMP-free strain. We also found that the cdaA mutant has an increased sensitivity against isoleucine. The isoleucine-dependent growth inhibition of the cdaA mutant is suppressed by codY mutations that likely reduce the DNA-binding activity of encoded CodY variants. Moreover, the characterization of the cdaA suppressor mutants revealed that the Opp oligopeptide transport system is involved in the uptake of the antibiotic fosfomycin. In conclusion, the suppressor analysis corroborates a key function of c-di-AMP in controlling osmolyte homeostasis in L. monocytogenes.
Author Schwedt, Inge
Commichau, Fabian M.
Holland, Gudrun
Halbedel, Sven
Gibhardt, Johannes
Scheibner, Katrin
Wang, Mengyi
Wamp, Sabrina
Schmidtke, Kai‐Uwe
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Snippet Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH...
The human pathogen Listeria monocytogenes synthesizes and degrades c-di-AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH...
Summary The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH...
The human pathogen Listeria monocytogenes synthesizes and degrades c‐di‐AMP using the diadenylate cyclase CdaA and the phosphodiesterases PdeA and PgpH...
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SubjectTerms AMP
Antibiotics
Bacteria
Defects
Deoxyribonucleic acid
DNA
Fosfomycin
Growth
Homeostasis
Isoleucine
Listeria
Listeria monocytogenes
Metabolism
Mutation
Pathogens
Perturbation
Phenotypes
Suppressor mutant
Transportation systems
Uptake
Title Adaptation of Listeria monocytogenes to perturbation of c‐di‐AMP metabolism underpins its role in osmoadaptation and identifies a fosfomycin uptake system
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1462-2920.16084
https://www.ncbi.nlm.nih.gov/pubmed/35688634
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https://search.proquest.com/docview/2675601220
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