A protease and a lipoprotein jointly modulate the conserved ExoR-ExoS-ChvI signaling pathway critical in Sinorhizobium meliloti for symbiosis with legume hosts
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Published:2023-10-23
Issue:10
Volume:19
Page:e1010776
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ISSN:1553-7404
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Container-title:PLOS Genetics
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language:en
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Short-container-title:PLoS Genet
Author:
Bustamante Julian A.ORCID,
Ceron Josue S.ORCID,
Gao Ivan Thomas,
Ramirez Hector A.,
Aviles Milo V.ORCID,
Bet Adam DemsinORCID,
Brice Jason R.ORCID,
Cuellar Rodrigo A.ORCID,
Dockery Eva,
Jabagat Miguel KarloORCID,
Karp Donna Grace,
Lau Joseph Kin-OnORCID,
Li SulingORCID,
Lopez-Magaña RaymondoORCID,
Moore Rebecca R.ORCID,
Morin Bethany Kristi R.,
Nzongo JulianaORCID,
Rezaeihaghighi YashaORCID,
Sapienza-Martinez JosephORCID,
Tran Tuyet Thi KimORCID,
Huang Zhenzhong,
Duthoy Aaron J.,
Barnett Melanie J.ORCID,
Long Sharon R.ORCID,
Chen Joseph C.ORCID
Abstract
Sinorhizobium meliloti is a model alpha-proteobacterium for investigating microbe-host interactions, in particular nitrogen-fixing rhizobium-legume symbioses. Successful infection requires complex coordination between compatible host and endosymbiont, including bacterial production of succinoglycan, also known as exopolysaccharide-I (EPS-I). In S. meliloti EPS-I production is controlled by the conserved ExoS-ChvI two-component system. Periplasmic ExoR associates with the ExoS histidine kinase and negatively regulates ChvI-dependent expression of exo genes, necessary for EPS-I synthesis. We show that two extracytoplasmic proteins, LppA (a lipoprotein) and JspA (a lipoprotein and a metalloprotease), jointly influence EPS-I synthesis by modulating the ExoR-ExoS-ChvI pathway and expression of genes in the ChvI regulon. Deletions of jspA and lppA led to lower EPS-I production and competitive disadvantage during host colonization, for both S. meliloti with Medicago sativa and S. medicae with M. truncatula. Overexpression of jspA reduced steady-state levels of ExoR, suggesting that the JspA protease participates in ExoR degradation. This reduction in ExoR levels is dependent on LppA and can be replicated with ExoR, JspA, and LppA expressed exogenously in Caulobacter crescentus and Escherichia coli. Akin to signaling pathways that sense extracytoplasmic stress in other bacteria, JspA and LppA may monitor periplasmic conditions during interaction with the plant host to adjust accordingly expression of genes that contribute to efficient symbiosis. The molecular mechanisms underlying host colonization in our model system may have parallels in related alpha-proteobacteria.
Funder
National Institute of General Medical Sciences
Division of Integrative Organismal Systems
Division of Biological Infrastructure
Arnold and Mabel Beckman Foundation
Publisher
Public Library of Science (PLoS)
Subject
Cancer Research,Genetics (clinical),Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics