Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa

Pseudomonas aeruginosa causes many biofilm infections, and the rugose small-colony variants (RSCVs) of this bacterium are important for infection. We found here that inactivation of PA2444, which we determined to be a serine hydroxymethyltransferase (SHMT), leads to the RSCV phenotype of P. aerugino...

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Main Authors: Mingming Pu, Lili Sheng, Sooyeon Song, Ting Gong, Thomas K. Wood
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2018.00315/full
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spelling doaj-cab3923edacf40bd8a5d7627793e5e7f2020-11-24T22:56:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-02-01910.3389/fmicb.2018.00315339551Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosaMingming PuLili ShengSooyeon SongTing GongThomas K. WoodPseudomonas aeruginosa causes many biofilm infections, and the rugose small-colony variants (RSCVs) of this bacterium are important for infection. We found here that inactivation of PA2444, which we determined to be a serine hydroxymethyltransferase (SHMT), leads to the RSCV phenotype of P. aeruginosa PA14. In addition, loss of PA2444 increases biofilm formation by two orders of magnitude, increases exopolysaccharide by 45-fold, and abolishes swarming. The RSCV phenotype is related to higher cyclic diguanylate concentrations due to increased activity of the Wsp chemosensory system, including diguanylate cyclase WspR. By characterizing the PA2444 enzyme in vitro, we determined the physiological function of PA2444 protein by relating it to S-adenosylmethionine (SAM) concentrations and methylation of a membrane bound methyl-accepting chemotaxis protein WspA. A whole transcriptome analysis also revealed PA2444 is related to the redox state of the cells, and the altered redox state was demonstrated by an increase in the intracellular NADH/NAD+ ratio. Hence, we provide a mechanism for how an enzyme of central metabolism controls the community behavior of the bacterium, and suggest the PA2444 protein should be named ShrA for serine hydroxymethyltransferase related to rugose colony formation.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00315/fullrugosesmall colony variantsserine hydroxymethyltransferasePseudomonas aeruginosabiofilm formation
collection DOAJ
language English
format Article
sources DOAJ
author Mingming Pu
Lili Sheng
Sooyeon Song
Ting Gong
Thomas K. Wood
spellingShingle Mingming Pu
Lili Sheng
Sooyeon Song
Ting Gong
Thomas K. Wood
Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
Frontiers in Microbiology
rugose
small colony variants
serine hydroxymethyltransferase
Pseudomonas aeruginosa
biofilm formation
author_facet Mingming Pu
Lili Sheng
Sooyeon Song
Ting Gong
Thomas K. Wood
author_sort Mingming Pu
title Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
title_short Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
title_full Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
title_fullStr Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
title_full_unstemmed Serine Hydroxymethyltransferase ShrA (PA2444) Controls Rugose Small-Colony Variant Formation in Pseudomonas aeruginosa
title_sort serine hydroxymethyltransferase shra (pa2444) controls rugose small-colony variant formation in pseudomonas aeruginosa
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-02-01
description Pseudomonas aeruginosa causes many biofilm infections, and the rugose small-colony variants (RSCVs) of this bacterium are important for infection. We found here that inactivation of PA2444, which we determined to be a serine hydroxymethyltransferase (SHMT), leads to the RSCV phenotype of P. aeruginosa PA14. In addition, loss of PA2444 increases biofilm formation by two orders of magnitude, increases exopolysaccharide by 45-fold, and abolishes swarming. The RSCV phenotype is related to higher cyclic diguanylate concentrations due to increased activity of the Wsp chemosensory system, including diguanylate cyclase WspR. By characterizing the PA2444 enzyme in vitro, we determined the physiological function of PA2444 protein by relating it to S-adenosylmethionine (SAM) concentrations and methylation of a membrane bound methyl-accepting chemotaxis protein WspA. A whole transcriptome analysis also revealed PA2444 is related to the redox state of the cells, and the altered redox state was demonstrated by an increase in the intracellular NADH/NAD+ ratio. Hence, we provide a mechanism for how an enzyme of central metabolism controls the community behavior of the bacterium, and suggest the PA2444 protein should be named ShrA for serine hydroxymethyltransferase related to rugose colony formation.
topic rugose
small colony variants
serine hydroxymethyltransferase
Pseudomonas aeruginosa
biofilm formation
url http://journal.frontiersin.org/article/10.3389/fmicb.2018.00315/full
work_keys_str_mv AT mingmingpu serinehydroxymethyltransferaseshrapa2444controlsrugosesmallcolonyvariantformationinpseudomonasaeruginosa
AT lilisheng serinehydroxymethyltransferaseshrapa2444controlsrugosesmallcolonyvariantformationinpseudomonasaeruginosa
AT sooyeonsong serinehydroxymethyltransferaseshrapa2444controlsrugosesmallcolonyvariantformationinpseudomonasaeruginosa
AT tinggong serinehydroxymethyltransferaseshrapa2444controlsrugosesmallcolonyvariantformationinpseudomonasaeruginosa
AT thomaskwood serinehydroxymethyltransferaseshrapa2444controlsrugosesmallcolonyvariantformationinpseudomonasaeruginosa
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