Multicopy single-stranded DNA directs intestinal colonization of enteric pathogens

Elfenbein, Johanna R.; Knodler, Leigh A.; Nakayasu, Ernesto S.; Ansong, Charles; Brewer, Heather M.; Bogomolnaya, Lydia; Adams, L. Garry; McClelland, Michael; Adkins, Joshua N.; Andrews-Polymenis, Helene L.; Fang, Ferric C.

doi:10.1371/journal.pgen.1005472

Title: Multicopy single-stranded DNA directs intestinal colonization of enteric pathogens

Journal Article · 13 September 2015 · PLoS Genetics

DOI: https://doi.org/10.1371/journal.pgen.1005472 · OSTI ID:1214726

Elfenbein, Johanna R. ^[1]; Knodler, Leigh A. ^[2]; Nakayasu, Ernesto S. ^[3]; Ansong, Charles ^[4]; Brewer, Heather M. ^[4]; Bogomolnaya, Lydia ^[5]; Adams, L. Garry ^[5]; McClelland, Michael ^[6]; Adkins, Joshua N. ^[4]; Andrews-Polymenis, Helene L. ^[5]; Fang, Ferric C. ^[7]

Texas A & M Univ., College Station, TX (United States); North Carolina State Univ., Raleigh, NC (United States)
Washington State Univ., Pullman, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Purdue Univ., West Lafayette, IN (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Texas A & M Univ., College Station, TX (United States)
Univ. of California-Irvine, Irvine, CA (United States)
Univ. of Washington, Seattle, WA (United States)

Multicopy single-stranded DNAs (msDNAs) are hybrid RNA-DNA molecules encoded on retroelements called retrons and produced by the action of retron reverse transcriptases. Retrons are widespread in bacteria but the natural function of msDNA has remained elusive despite 30 years of study. The major roadblock to elucidation of the function of these unique molecules has been the lack of any identifiable phenotypes for mutants unable to make msDNA. We report that msDNA of the zoonotic pathogen Salmonella Typhimurium is necessary for colonization of the intestine. Similarly, we observed a defect in intestinal persistence in an enteropathogenic E. coli mutant lacking its retron reverse transcriptase. Under anaerobic conditions in the absence of msDNA, proteins of central anaerobic metabolism needed for Salmonella colonization of the intestine are dysregulated. We show that the msDNA-deficient mutant can utilize nitrate, but not other alternate electron acceptors in anaerobic conditions. Consistent with the availability of nitrate in the inflamed gut, a neutrophilic inflammatory response partially rescued the ability of a mutant lacking msDNA to colonize the intestine. These findings together indicate that the mechanistic basis of msDNA function during Salmonella colonization of the intestine is proper production of proteins needed for anaerobic metabolism. We further conclude that a natural function of msDNA is to regulate protein abundance, the first attributable function for any msDNA. Our data provide novel insight into the function of this mysterious molecule that likely represents a new class of regulatory molecules.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1214726

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 9 Vol. 11; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Data from: Multicopy single-stranded DNA directs intestinal colonization of enteric pathogens Elfenbein, Johanna R.; Knodler, Leigh A.; Nakayasu, Ernesto S. Dryad https://doi.org/10.5061/dryad.ph81m	dataset	January 2016
Multiple mechanisms drive phage infection efficiency in nearly identical hosts Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0099-8	journal	March 2018
Retrons and their applications in genome engineering Simon, Anna J.; Ellington, Andrew D.; Finkelstein, Ilya J. Nucleic Acids Research, Vol. 47, Issue 21 https://doi.org/10.1093/nar/gkz865	journal	October 2019
Ancient Regulatory Role of Lysine Acetylation in Central Metabolism Nakayasu, Ernesto S.; Burnet, Meagan C.; Walukiewicz, Hanna E. mBio, Vol. 8, Issue 6 https://doi.org/10.1128/mbio.01894-17	journal	November 2017
A Salmonella Regulator Modulates Intestinal Colonization and Use of Phosphonoacetic Acid Elfenbein, Johanna R.; Knodler, Leigh A.; Schaeffer, Allison R. Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00069	journal	March 2017
Data from: Multicopy single-stranded DNA directs intestinal colonization of enteric pathogens Elfenbein, Johanna R.; Knodler, Leigh A.; Nakayasu, Ernesto S. Dryad https://doi.org/10.5061/dryad.ph81m	dataset	January 2016

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