Host-emitted amino acid cues regulate bacterial chemokinesis to enhance colonization

Robinson, Catherine D.; Sweeney, Emily Goers; Ngo, Julia; Ma, Emily; Perkins, Arden; Smith, T. Jarrod; Fernandez, Nicolas L.; Waters, Christopher M.; Remington, S.J.; Bohannan, Brendan J. M.; Guillemin, Karen

doi:10.1016/j.chom.2021.06.003

Cited by 32 publications

(22 citation statements)

References 89 publications

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“…This distribution of Aer01 in fixed tissue mirrors previous live imaging observations of Aer01 colonization dynamics (Schlomann et al, 2019; Wiles et al, 2016). The planktonic Aer01 may represent recently immigrated bacteria, as motility is critical for Aer01 immigration (Robinson et al, 2018, 2021). Additionally, we observed small Aer01 aggregates in the same region as mucus in the distal midgut lumen ( Fig.…”

Section: Resultsmentioning

confidence: 99%

A mucin-regulated adhesin determines the intestinal biogeography and inflammatory character of a bacterial symbiont

Smith

Sundarraman

Melançon

et al. 2022

Preprint

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In a healthy gut, microbes are often aggregated with host mucus, yet the molecular basis for this organization and its impact on intestinal health are unclear. Mucus is a viscous physical barrier separating resident microbes from epithelia, but also provides glycan cues that regulate microbial behaviors. Using experimental evolution, we discovered a mucin-sensing pathway in an Aeromonas symbiont of zebrafish, Aer01. In response to the mucin-associated glycan N-acetylglucosamine, a sensor kinase regulates expression of a mucin-binding adhesin we named MbpA. When MbpA is disrupted, Aer01 colonizes to normal levels, but is largely planktonic and elicits increased intestinal inflammation, traits which are reversed by increasing cell surface MpbA. MbpA-like adhesins are common in human-associated bacteria and expression of an Akkermansia muciniphila MbpA-like adhesin in MbpA-deficient Aer01 restored lumenal aggregation and reversed its pro-inflammatory character. Our work demonstrates how resident bacteria use mucin glycans to modulate behaviors congruent with host health.

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Section: Resultsmentioning

confidence: 99%

A mucin-regulated adhesin determines the intestinal biogeography and inflammatory character of a bacterial symbiont

Smith

Sundarraman

Melançon

et al. 2022

Preprint

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“…There are also likely to be beneficial symbiosis-specific adaptations within c-di-GMP signaling. For example, the zebrafish gut symbiont Aeromonas veronii responds to host amino acids to inhibit a diguanylate cyclase, thereby stimulating bacterial motility into the host (Robinson et al, 2021). It remains to be seen whether there are similar specific adaptations in the V. fischeri -squid symbiosis.…”

Section: Discussionmentioning

confidence: 99%

High levels of cyclic diguanylate interfere with beneficial bacterial colonization

Isenberg

Christensen

Visick

et al. 2022

Preprint

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During colonization of the Hawaiian bobtail squid (Euprymna scolopes), Vibrio fischeri bacteria undergo a lifestyle transition from a planktonic motile state in the environment to a biofilm state in host mucus. Cyclic diguanylate (c-di-GMP) is a cytoplasmic signaling molecule that is important for regulating motility-biofilm transitions in many bacterial species. V. fischeri encodes 50 proteins predicted to synthesize and/or degrade c-di-GMP, but a role for c-di-GMP regulation during host colonization has not been investigated. We examined strains exhibiting either low or high levels of c-di-GMP during squid colonization and found that while a low c-di-GMP strain had no colonization defect, a high c-di-GMP strain was severely impaired. Expression of a heterologous c-di-GMP phosphodiesterase restored colonization, demonstrating that the effect is due to high c-di-GMP levels. In the constitutive high c-di-GMP state, colonizing V. fischeri exhibited reduced motility, altered biofilm aggregate morphology, and a transcriptional regulatory interaction between two key polysaccharides, cellulose and Syp. Our results highlight the importance of proper c-di-GMP regulation during beneficial animal colonization, illustrate multiple pathways regulated by c-di-GMP in the host, and uncover an interplay of multiple exopolysaccharide systems in host-associated aggregates.

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“…Another recent discovery exemplifies amino acid sensing. SpdE from Aeromonas veronii is a DGC that uses a dCACHE_1 domain to sense proline, valine, and isoleucine ( 197 ). Structural analysis revealed that the amino acid ligands bind to the dCACHE_1 domain via a series of critical amino acid residues in a binding pocket that can fit only small hydrophobic amino acids.…”

Section: Making Sense Of It All: the Sensory Functions Of C-di-gmp Ne...mentioning

confidence: 99%

“…Proline, valine, and isoleucine inhibit SpdE DGC activity, directly increasing the speed of cells, as measured by microscopy. This process, called chemokinesis, works in concert with chemotaxis to facilitate the rapid movement of A. veronii into the host in the presence of SpdE-inhibiting ligands ( 197 ).…”

Section: Making Sense Of It All: the Sensory Functions Of C-di-gmp Ne...mentioning

confidence: 99%

Sensory Perception in Bacterial Cyclic Diguanylate Signal Transduction

et al. 2022

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Cyclic diguanylate (c-di-GMP) signal transduction systems provide bacteria the ability to sense changing cell status or environmental conditions and then execute suitable physiological and social behaviours in response. In this review, we provide a comprehensive census of the stimuli and receptors that are linked to modulation of intracellular c-di-GMP. Emerging evidence indicates that c-di-GMP networks sense light, surfaces, energy, redox potential, respiratory electron acceptors, temperature, and structurally diverse biotic and abiotic chemicals. Bioinformatic analysis of sensory domains in diguanylate cyclases and c-di-GMP-specific phosphodiesterases as well as the receptor complexes associated with them reveals that these functions are linked to a diverse repertoire of protein domain families. We describe the principles of stimulus perception learned from studying these modular sensory devices, illustrate how they are assembled in varied combinations with output domains, and summarize a system for classifying these sensor proteins based on their complexity. Biological information-processing via c-di-GMP signal transduction is not only fundamental to bacterial survival in dynamic environments, but also is being used to engineer gene expression circuitry and synthetic proteins with à la carte biochemical functionalities.

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Host-emitted amino acid cues regulate bacterial chemokinesis to enhance colonization

Cited by 32 publications

References 89 publications

A mucin-regulated adhesin determines the intestinal biogeography and inflammatory character of a bacterial symbiont

A mucin-regulated adhesin determines the intestinal biogeography and inflammatory character of a bacterial symbiont

High levels of cyclic diguanylate interfere with beneficial bacterial colonization

Sensory Perception in Bacterial Cyclic Diguanylate Signal Transduction

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