Acidic pH promotes lipopolysaccharide modification and alters colonization in a bacteria–animal mutualism

Schwartzman, Julia; Lynch, Jonathan B.; Ramos, Stephany Flores; Zhou, Lawrence; Apicella, Michael A.; Yew, Joanne Y.; Ruby, Edward G.

doi:10.1111/mmi.14365

Cited by 16 publications

(11 citation statements)

References 75 publications

(82 reference statements)

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“…This study, along with other work from our group (126), positions H-NS as a previously underappreciated regulator of diverse symbiotic phenotypes in V. fischeri. Specifically, H-NS suppresses luminescence in both V. fischeri (90) and Photobacterium leiognathi (111) and regulates ompU (Fig.…”

Section: Discussionsupporting

confidence: 59%

“…fischeri OMVs have different levels of OmpU depending on culture pH. Previous transcriptional analyses discovered that several predicted membrane components of V. fischeri cells were differentially expressed at distinct pHs (126). We hypothesized that the pH shifts characteristic of the transition that V. fischeri cells experience between planktonic and host-associated lifestyles would induce changes in the molecular composition of their OMVs as well and that such changes would affect the ability of these vesicles to trigger developmental responses in the newly colonized juvenile squid.…”

Section: Resultsmentioning

confidence: 99%

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Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

et al. 2019

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Outer membrane vesicles (OMVs) are continuously produced by Gram-negative bacteria and are increasingly recognized as ubiquitous mediators of bacterial physiology. In particular, OMVs are powerful effectors in interorganismal interactions, driven largely by their molecular contents. These impacts have been studied extensively in bacterial pathogenesis but have not been well documented within the context of mutualism. Here, we examined the proteomic composition of OMVs from the marine bacterium Vibrio fischeri, which forms a specific mutualism with the Hawaiian bobtail squid, Euprymna scolopes. We found that V. fischeri upregulates transcription of its major outer membrane protein, OmpU, during growth at an acidic pH, which V. fischeri experiences when it transitions from its environmental reservoir to host tissues. We used comparative genomics and DNA pulldown analyses to search for regulators of ompU and found that differential expression of ompU is governed by the OmpR, H-NS, and ToxR proteins. This transcriptional control combines with nutritional conditions to govern OmpU levels in OMVs. Under a host-encountered acidic pH, V. fischeri OMVs become more potent stimulators of symbiotic host development in an OmpU-dependent manner. Finally, we found that symbiotic development could be stimulated by OMVs containing a homolog of OmpU from the pathogenic species Vibrio cholerae, connecting the role of a well-described virulence factor with a mutualistic element. This work explores the symbiotic effects of OMV variation, identifies regulatory machinery shared between pathogenic and mutualistic bacteria, and provides evidence of the role that OMVs play in animal-bacterium mutualism. IMPORTANCE Beneficial bacteria communicate with their hosts through a variety of means. These communications are often carried out by a combination of molecules that stimulate responses from the host and are necessary for development of the relationship between these organisms. Naturally produced bacterial outer membrane vesicles (OMVs) contain many of those molecules and can stimulate a wide range of responses from recipient organisms. Here, we describe how a marine bacterium, Vibrio fischeri, changes the makeup of its OMVs under conditions that it experiences as it goes from its free-living lifestyle to associating with its natural host, the Hawaiian bobtail squid. This work improves our understanding of how bacteria change their signaling profile as they begin to associate with their beneficial partner animals.

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Section: Discussionsupporting

confidence: 59%

Section: Resultsmentioning

confidence: 99%

Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

et al. 2019

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“…3 ). While lipopolysaccharide and the syp polysaccharide have been implicated in the initiation of host colonization by V. fischeri ( 38 – 40 ), little has been determined regarding the possible involvement of extracellular polysaccharides in colonization persistence. V. fischeri -colonized crypts, despite having no goblet cells (S. V. Nyholm, personal communication), have been shown to stain alcian blue positive ( 41 ), indicating that the presumptive EPS made by VF_0157–80 may be a relevant factor in E. scolopes - V. fischeri symbiosis.…”

Section: Discussionmentioning

confidence: 99%

HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in Vibrio fischeri

Bennett

Essock‐Burns

Ruby

2020

mBio

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The bioluminescent bacterium Vibrio fischeri forms a mutually beneficial symbiosis with the Hawaiian bobtail squid, Euprymna scolopes, in which the bacteria, housed inside a specialized light organ, produce light used by the squid in its nocturnal activities. Upon hatching, E. scolopes juveniles acquire V. fischeri from the seawater through a complex process that requires, among other factors, chemotaxis by the bacteria along a gradient of N-acetylated sugars into the crypts of the light organ, the niche in which the bacteria reside. Once inside the light organ, V. fischeri transitions into a symbiotic, sessile state in which the quorum-signaling regulator LitR induces luminescence. In this work we show that expression of litR and luminescence are repressed by a homolog of the Vibrio cholerae virulence factor TcpP, which we have named HbtR. Further, we demonstrate that LitR represses genes involved in motility and chemotaxis into the light organ and activates genes required for exopolysaccharide production. IMPORTANCE TcpP homologs are widespread throughout the Vibrio genus; however, the only protein in this family described thus far is a V. cholerae virulence regulator. Here, we show that HbtR, the TcpP homolog in V. fischeri, has both a biological role and regulatory pathway completely unlike those in V. cholerae. Through its repression of the quorum-signaling regulator LitR, HbtR affects the expression of genes important for colonization of the E. scolopes light organ. While LitR becomes activated within the crypts and upregulates luminescence and exopolysaccharide genes and downregulates chemotaxis and motility genes, it appears that HbtR, upon expulsion of V. fischeri cells into seawater, reverses this process to aid the switch from a symbiotic to a planktonic state. The possible importance of HbtR to the survival of V. fischeri outside its animal host may have broader implications for the ways in which bacteria transition between often vastly different environmental niches.

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“…Animal‐associated microbes can experience spatio‐temporal variations in nutrient availability and antagonism from host defences or competing microbes (van der Woude and Bäumler, 2004; Veening et al ., 2008; Bury‐Moné and Sclavi, 2017; Cao et al ., 2017; Cao and Goodrich‐Blair, 2017; Sánchez‐Romero and Casadesús, 2018; Schwartzman et al ., 2019). To promote success in fluctuating environments, some host‐associated microbes have evolved mechanisms of phenotypic variation or plasticity.…”

Section: Introductionmentioning

confidence: 99%

Xenorhabdus nematophila bacteria shift from mutualistic to virulent Lrp‐dependent phenotypes within the receptacles of Steinernema carpocapsae insect‐infective stage nematodes

Cao

Goodrich‐Blair

2020

Environmental Microbiology

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Xenorhabdus nematophila bacteria are mutualists of Steinernema carpocapsae nematodes and pathogens of insects. Xenorhabdus nematophila exhibits phenotypic variation between insect virulence (V) and the mutualistic (M) support of nematode reproduction and colonization initiation in the infective juvenile (IJ) stage nematode that carries X. nematophila between insect hosts. The V and M phenotypes occur reciprocally depending on levels of the transcription factor Lrp: high-Lrp expressors are M+V− while low-Lrp expressors are V+M−. We report here that variable (wild type) or fixed high-Lrp expressors also are optimized, relative to low-or no-Lrp expressors, for colonization of additional nematode stages: juvenile, adult and pre-transmission infective juvenile (IJ). In contrast, we found that after the bacterial population had undergone outgrowth in mature IJs, the advantage for colonization shifted to low-Lrp expressors: fixed low-Lrp expressors (M−V+) and wild type (M+V +) exhibited higher average bacterial CFU per IJ than did high-Lrp (M+V−) or no-Lrp (M−V−) strains. Further, the bacterial population becomes increasingly low-Lrp expressing, based on expression of an Lrpdependent fluorescent reporter, as IJs age. These data support a model that virulent X. nematophila have a selective advantage and accumulate in aging IJs in advance of exposure to insect hosts in which this phenotype is necessary.

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Acidic pH promotes lipopolysaccharide modification and alters colonization in a bacteria–animal mutualism

Cited by 16 publications

References 75 publications

Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in Vibrio fischeri

Xenorhabdus nematophila bacteria shift from mutualistic to virulent Lrp‐dependent phenotypes within the receptacles of Steinernema carpocapsae insect‐infective stage nematodes

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