Genetic analysis of signal integration by the Sinorhizobium meliloti sensor kinase FeuQ

VanYperen, Ryan D.; Orton, Taylor S.; Griffitts, Joel S.

doi:10.1099/mic.0.000002

“…Nevertheless, other possible explanations, not mutually exclusive, can also account for JspA's involvement in resistance against cell envelope assaults: for example, JspA may degrade other substrates or signaling pathways under specific conditions, or JspA and LppA may assist in the proper construction of the cell envelope by ensuring proper maturation of other lipoproteins. Furthermore, a number of other signaling systems, such as ActK-ActJ, CenK-CenR, CpxA-CpxR, EmmB-EmmC, FeuQ-FeuP, and NtrX-NtrY, contribute to the maintenance of cell envelope integrity in rhizobia (Albicoro et al, 2021;Albicoro et al, 2023;Bensig et al, 2022;Calatrava-Morales et al, 2017;Lakey et al, 2022;Morris & Gonzalez, 2009;Santos et al, 2010;VanYperen et al, 2015;Wang et al, 2013;Xing et al, 2022), and how these different systems cooperate with ExoS-ChvI to ensure successful symbiosis remains ripe for further investigation.…”

Section: Discussionmentioning

confidence: 99%

A protease and a lipoprotein jointly modulate the conserved ExoR-ExoS-ChvI signaling pathway critical inSinorhizobium melilotifor symbiosis with legume hosts

Bustamante,

Ceron,

Gao

et al. 2023

Preprint

0

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Sinorhizobium melilotiis 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). InS. melilotiEPS-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 ofexogenes, necessary for EPS-I synthesis. We show that two extracytoplasmic proteins, LppA (a lipoprotein) and JspA (a metalloprotease), jointly influence EPS-I synthesis by modulating the ExoR-ExoS-ChvI pathway and expression of genes in the ChvI regulon. Deletions ofjspAandlppAled to lower EPS-I production and competitive disadvantage during host colonization, for bothS. melilotiwithMedicago sativaandS. medicaewithM. truncatula. Overexpression ofjspAreduced 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 inCaulobacter crescentusandEscherichia 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.Author summarySymbiotic bacteria that live in the roots of legume plants produce biologically accessible nitrogen compounds, offering a more sustainable and environmentally sound alternative to industrial fertilizers generated from fossil fuels. Understanding the multitude of factors that contribute to successful interaction between such bacteria and their plant hosts can help refine strategies for improving agricultural output. In addition, because disease-causing microbes share many genes with these beneficial bacteria, unraveling the cellular mechanisms that facilitate host invasion can reveal ways to prevent and treat infectious diseases. In this report we show that two genes in the model bacteriumSinorhizobium meliloticontribute to effective symbiosis by helping the cells adapt to living in host plants. This finding furthers knowledge about genetics factors that regulate interactions between microbes and their hosts.

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“…Thus, MgrB drives the inactivation of PhoP by PhoQ, forming a feedback loop (Lippa and Goulian, ; Salazar et al, ); (ii) the Sinorhizobium meliloti FeuN protein, a 83 amino acids long periplasmic protein, interacts directly with the periplasmic domain of the FeuQ SHK, resulting in increased phosphatase activity against its cognate RR FeuP. Thus, FeuN drives the inactivation of FeuP by FeuQ (Carlyon et al, ; VanYperen et al, ); (iii) the S. enterica CacA protein, a 63 amino acids long predicted cytoplasmic protein, which is regulated by RssB and RpoS and activates the CpxRA TCS using an unknown mechanism (Kato et al, ). All the connectors/modulators described here are small proteins, they are located in the cytoplasm, inner membrane or periplasm, they activate or repress the activity of their target TCS, they function on the RR or SHK component of their target TCS, they affect the function of their target component using different mechanisms and beside LerC they share no sequence homology with other proteins.…”

Section: Discussionmentioning

confidence: 99%

The single‐domain response regulator LerC functions as a connector protein in the Legionella pneumophila effectors regulatory network

Feldheim

¹

,

Zusman

²

,

Kapach

³

et al. 2018

Molecular Microbiology

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The intracellular pathogen Legionella pneumophila translocates more than 300 effector proteins into host cells during infection. The PmrAB two-component system (TCS) has been shown to activate the expression of a large pool of these effector-encoding genes (EEGs) and the LetAS TCS, as part of the LetAS-RsmYZ-CsrA cascade, has been shown to repress the expression of another pool of EEGs. We identified a single-domain response regulator (SDRR), named LerC, which functions as a connector protein between the PmrAB and the LetAS TCSs. The lerC gene is strongly activated by the PmrAB TCS and the LerC protein inhibits the activity of the LetAS TCS. The LerC protein specifically interacts with the HPT (histidine-phosphotransfer) domain of LetS, leading to reduced expression of the small RNAs RsmY and RsmZ, which leads to a reduced expression of the pool of EEGs regulated by the LetAS-RsmYZ-CsrA cascade. In addition, the conserved aspartic acid located in the LerC receiver domain is essential for its phosphorylation and function, suggesting that LerC functions as a phosphate-sink of LetS. Our results demonstrate a new role for SDRRs as connector proteins in regulatory networks, suggesting that members of this widespread group of proteins might function as connector proteins in other bacterial regulatory networks.

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“…Nevertheless, other possible explanations, not mutually exclusive, can also account for JspA's involvement in resistance against cell envelope assaults: for example, JspA may degrade other substrates or signaling pathways under specific conditions, or JspA and LppA may assist in the proper construction of the cell envelope by ensuring proper maturation of other lipoproteins. Furthermore, a number of other signaling systems, such as ActK-ActJ, CenK-CenR, CpxA-CpxR, EmmB-EmmC, FeuQ-FeuP, and NtrX-NtrY, contribute to the maintenance of cell envelope integrity in S. meliloti [46,55,[134][135][136][137][138][139][140][141][142][143], and how these different systems cooperate with ExoS-ChvI to ensure successful symbiosis remains ripe for further investigation.…”

Section: Plos Geneticsmentioning

confidence: 99%

A protease and a lipoprotein jointly modulate the conserved ExoR-ExoS-ChvI signaling pathway critical in Sinorhizobium meliloti for symbiosis with legume hosts

Bustamante,

Ceron,

Gao

et al. 2023

View full text Add to dashboard Cite

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.

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Genetic analysis of signal integration by the Sinorhizobium meliloti sensor kinase FeuQ

Cited by 4 publications

References 38 publications

A protease and a lipoprotein jointly modulate the conserved ExoR-ExoS-ChvI signaling pathway critical inSinorhizobium melilotifor symbiosis with legume hosts

A protease and a lipoprotein jointly modulate the conserved ExoR-ExoS-ChvI signaling pathway critical inSinorhizobium melilotifor symbiosis with legume hosts

The single‐domain response regulator LerC functions as a connector protein in the Legionella pneumophila effectors regulatory network

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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