Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli

ABSTRACT Escherichia coli associates with humans early in life and can occupy several body niches either as a commensal in the gut and vagina, or as a pathogen in the urinary tract. As such, E. coli has an arsenal of acid response mechanisms that allow it to withstand the different levels of acid st...

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Main Authors: Michelle A. Wiebe, John R. Brannon, Bradley D. Steiner, Adebisi Bamidele, Alexandra C. Schrimpe-Rutledge, Simona G. Codreanu, Stacy D. Sherrod, John A. McLean, Maria Hadjifrangiskou
Format: Article
Language:English
Published: American Society for Microbiology 2022-12-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.02963-22
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author Michelle A. Wiebe
John R. Brannon
Bradley D. Steiner
Adebisi Bamidele
Alexandra C. Schrimpe-Rutledge
Simona G. Codreanu
Stacy D. Sherrod
John A. McLean
Maria Hadjifrangiskou
author_facet Michelle A. Wiebe
John R. Brannon
Bradley D. Steiner
Adebisi Bamidele
Alexandra C. Schrimpe-Rutledge
Simona G. Codreanu
Stacy D. Sherrod
John A. McLean
Maria Hadjifrangiskou
author_sort Michelle A. Wiebe
collection DOAJ
description ABSTRACT Escherichia coli associates with humans early in life and can occupy several body niches either as a commensal in the gut and vagina, or as a pathogen in the urinary tract. As such, E. coli has an arsenal of acid response mechanisms that allow it to withstand the different levels of acid stress encountered within and outside the host. Here, we report the discovery of an additional acid response mechanism that involves the deamination of l-serine to pyruvate by the conserved l-serine deaminases SdaA and SdaB. l-serine is the first amino acid to be imported in E. coli during growth in laboratory media. However, there remains a lack in knowledge as to how l-serine is utilized. Using a uropathogenic strain of E. coli, UTI89, we show that in acidified media, l-serine is brought into the cell via the SdaC transporter. We further demonstrate that deletion of the l-serine deaminases SdaA and SdaB renders E. coli susceptible to acid stress, similar to other acid stress deletion mutants. The pyruvate produced by l-serine deamination activates the pyruvate sensor BtsS, which in concert with the noncognate response regulator YpdB upregulates the putative transporter YhjX. Based on these observations, we propose that l-serine deamination constitutes another acid response mechanism in E. coli. IMPORTANCE The observation that l-serine uptake occurs as E. coli cultures grow is well established, yet the benefit E. coli garners from this uptake remains unclear. Here, we report a novel acid tolerance mechanism where l-serine is deaminated to pyruvate and ammonia, promoting survival of E. coli under acidic conditions. This study is important as it provides evidence of the use of l-serine as an acid response strategy, not previously reported for E. coli.
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spelling doaj.art-94d3b34cefde4c1ba018ab558b5de37f2022-12-22T03:54:37ZengAmerican Society for MicrobiologymBio2150-75112022-12-0113610.1128/mbio.02963-22Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coliMichelle A. Wiebe0John R. Brannon1Bradley D. Steiner2Adebisi Bamidele3Alexandra C. Schrimpe-Rutledge4Simona G. Codreanu5Stacy D. Sherrod6John A. McLean7Maria Hadjifrangiskou8Vanderbilt University, Nashville, Tennessee, USADepartment of Pathology, Microbiology & Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USAVanderbilt University, Nashville, Tennessee, USADepartment of Pathology, Microbiology & Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USAABSTRACT Escherichia coli associates with humans early in life and can occupy several body niches either as a commensal in the gut and vagina, or as a pathogen in the urinary tract. As such, E. coli has an arsenal of acid response mechanisms that allow it to withstand the different levels of acid stress encountered within and outside the host. Here, we report the discovery of an additional acid response mechanism that involves the deamination of l-serine to pyruvate by the conserved l-serine deaminases SdaA and SdaB. l-serine is the first amino acid to be imported in E. coli during growth in laboratory media. However, there remains a lack in knowledge as to how l-serine is utilized. Using a uropathogenic strain of E. coli, UTI89, we show that in acidified media, l-serine is brought into the cell via the SdaC transporter. We further demonstrate that deletion of the l-serine deaminases SdaA and SdaB renders E. coli susceptible to acid stress, similar to other acid stress deletion mutants. The pyruvate produced by l-serine deamination activates the pyruvate sensor BtsS, which in concert with the noncognate response regulator YpdB upregulates the putative transporter YhjX. Based on these observations, we propose that l-serine deamination constitutes another acid response mechanism in E. coli. IMPORTANCE The observation that l-serine uptake occurs as E. coli cultures grow is well established, yet the benefit E. coli garners from this uptake remains unclear. Here, we report a novel acid tolerance mechanism where l-serine is deaminated to pyruvate and ammonia, promoting survival of E. coli under acidic conditions. This study is important as it provides evidence of the use of l-serine as an acid response strategy, not previously reported for E. coli.https://journals.asm.org/doi/10.1128/mbio.02963-22Escherichia coliacid stressbacterial stress responsemetabolomicsserine
spellingShingle Michelle A. Wiebe
John R. Brannon
Bradley D. Steiner
Adebisi Bamidele
Alexandra C. Schrimpe-Rutledge
Simona G. Codreanu
Stacy D. Sherrod
John A. McLean
Maria Hadjifrangiskou
Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
mBio
Escherichia coli
acid stress
bacterial stress response
metabolomics
serine
title Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
title_full Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
title_fullStr Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
title_full_unstemmed Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
title_short Serine Deamination Is a New Acid Tolerance Mechanism Observed in Uropathogenic Escherichia coli
title_sort serine deamination is a new acid tolerance mechanism observed in uropathogenic escherichia coli
topic Escherichia coli
acid stress
bacterial stress response
metabolomics
serine
url https://journals.asm.org/doi/10.1128/mbio.02963-22
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