An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa

Jeremiah N Marden; Manisha R Diaz; William G Walton; Cindy J Gode; Laurie Betts; Mark L Urbanowski; Matthew R Redinbo; Timothy L Yahr; Matthew C Wolfgang

doi:10.1073/pnas.1307217110

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An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa

Journal article

Open access

Peer reviewed

An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa

Jeremiah N Marden, Manisha R Diaz, William G Walton, Cindy J Gode, Laurie Betts, Mark L Urbanowski, Matthew R Redinbo, Timothy L Yahr and Matthew C Wolfgang

Proceedings of the National Academy of Sciences - PNAS, Vol.110(37), pp.15055-15060

09/10/2013

DOI: 10.1073/pnas.1307217110

PMCID: PMC3773774

PMID: 23980177

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Abstract

Members of the CsrA family of prokaryotic mRNA-binding proteins alter the translation and/or stability of transcripts needed for numerous global physiological processes. The previously described CsrA family member in Pseudomonas aeruginosa (RsmA) plays a central role in determining infection modality by reciprocally regulating processes associated with acute (type III secretion and motility) and chronic (type VI secretion and biofilm formation) infection. Here we describe a second, structurally distinct RsmA homolog in P. aeruginosa (RsmF) that has an overlapping yet unique regulatory role. RsmF deviates from the canonical 5 β-strand and carboxyl-terminal α-helix topology of all other CsrA proteins by having the α-helix internally positioned. Despite striking changes in topology, RsmF adopts a tertiary structure similar to other CsrA family members and binds a subset of RsmA mRNA targets, suggesting that RsmF activity is mediated through a conserved mechanism of RNA recognition. Whereas deletion of rsmF alone had little effect on RsmA-regulated processes, strains lacking both rsmA and rsmF exhibited enhanced RsmA phenotypes for markers of both type III and type VI secretion systems. In addition, simultaneous deletion of rsmA and rsmF resulted in superior biofilm formation relative to the wild-type or rsmA strains. We show that RsmF translation is derepressed in an rsmA mutant and demonstrate that RsmA specifically binds to rsmF mRNA in vitro, creating a global hierarchical regulatory cascade that operates at the posttranscriptional level.

Mutation

Protein Structure, Tertiary

Amino Acid Sequence

Genes, Bacterial

RNA-Binding Proteins - genetics

RNA Processing, Post-Transcriptional

RNA, Messenger - genetics

RNA-Binding Proteins - chemistry

Bacterial Proteins - chemistry

Bacterial Proteins - genetics

Biofilms - growth & development

Models, Molecular

Molecular Sequence Data

RNA, Messenger - metabolism

Regulon

Sequence Homology, Amino Acid

Pseudomonas aeruginosa - genetics

Pseudomonas aeruginosa - metabolism

Base Sequence

RNA, Bacterial - genetics

Bacterial Proteins - metabolism

RNA, Bacterial - metabolism

RNA-Binding Proteins - metabolism

Details

Title: Subtitle: An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa
Creators: Jeremiah N Marden - Cystic Fibrosis/Pulmonary Research and Treatment Center and Departments of Chemistry, Biochemistry and Biophysics, and Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599
Manisha R Diaz
William G Walton
Cindy J Gode
Laurie Betts
Mark L Urbanowski
Matthew R Redinbo
Timothy L Yahr
Matthew C Wolfgang
Resource Type: Journal article
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.110(37), pp.15055-15060
DOI: 10.1073/pnas.1307217110
PMID: 23980177
PMCID: PMC3773774
NLM abbreviation: Proc Natl Acad Sci U S A
ISSN: 1091-6490
eISSN: 1091-6490
Publisher: National Academy of Sciences; United States
Grant note: AI069116 / NIAID NIH HHS AI055042 / NIAID NIH HHS AI097264 / NIAID NIH HHS R01 AI055042 / NIAID NIH HHS R01 AI097264 / NIAID NIH HHS R01 AI069116 / NIAID NIH HHS
Language: English
Date published: 09/10/2013
Academic Unit: Microbiology and Immunology
Record Identifier: 9984001148402771

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