A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

Pan, Min; Schwartzman, Julia; Dunn, Anne K.; Zhang, Lu; Ruby, Edward G.

doi:10.1128/mbio.00811-15

Cited by 18 publications

(11 citation statements)

References 52 publications

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“…In the analysis, glpQ is the only gene specifically connected to the utilization of glycerophosphodiesters, because other genes involved in glycerol and G3P catabolism also play a role in the use of other nutrients. Overall, these results support the conclusion that nutrients such as NANA and glycerophosphodiester may be used as carbon sources by symbionts in the juvenile light organ (Pan et al ., ). Future metabolomics studies aimed at detecting these and other potential carbon sources in the host will help refine comparisons between our flux coupling analysis and transcriptomic results.…”

Section: Resultsmentioning

confidence: 97%

“…glycerophosphodiester may be used as carbon sources by symbionts in the juvenile light organ (Pan et al, 2015). Future metabolomics studies aimed at detecting these and other potential carbon sources in the host will help refine comparisons between our flux coupling analysis and transcriptomic results.…”

Section: Insight Into Symbiont Metabolism Within the Juvenile Hostmentioning

confidence: 99%

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Transcriptional characterization of Vibrio fischeri during colonization of juvenile Euprymna scolopes

Thompson

Nikolakakis

Pan

et al. 2017

Environmental Microbiology

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The marine bacterium Vibrio fischeri is the monospecific symbiont of the Hawaiian bobtail squid, Euprymna scolopes, and the establishment of this association involves a number of signaling pathways and transcriptional responses between both partners. We report here the first full RNA-Seq dataset representing host-associated V. fischeri cells from colonized juvenile E. scolopes, as well as comparative transcriptomes under both laboratory and simulated marine planktonic conditions. These data elucidate the broad transcriptional changes that these bacteria undergo during the early stages of symbiotic colonization. We report several previously undescribed and unexpected transcriptional responses within the early stages of this symbiosis, including gene expression patterns consistent with biochemical stresses inside the host, and metabolic patterns distinct from those reported in associations with adult animals. Integration of these transcriptional data with a recently developed metabolic model of V. fischeri provides us with a clearer picture of the metabolic state of symbionts within the juvenile host, including their possible carbon sources. Taken together, these results expand our understanding of the early stages of the squid–vibrio symbiosis, and more generally inform the transcriptional responses underlying the activities of marine microbes during host colonization.

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Section: Resultsmentioning

confidence: 97%

Section: Insight Into Symbiont Metabolism Within the Juvenile Hostmentioning

confidence: 99%

Transcriptional characterization of Vibrio fischeri during colonization of juvenile Euprymna scolopes

Thompson

Nikolakakis

Pan

et al. 2017

Environmental Microbiology

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“…The closely related vector-borne phytopathogenic bacterium Xylella fastidiosa enzymatically digests GlcNAc polymers (chitin) available in the foregut of the insect vector, also using the acquired GlcNAc as a nutrient source 39 . Remarkably, the effects of host-provided GlcNAc extend to the mutualistic association between bioluminescent squid and vibrio, where host-derived GlcNAc acts as a regulator of shifting the bacterial metabolism to provide optimal symbiont services to the host 40 . Determining the chemical identity of the bioactive molecule associated with NOPE1 remains an exciting future challenge, and whether NOPE1 contributes to microbe perception or influences root exudate composition requires further investigation.…”

Section: Discussionmentioning

confidence: 99%

An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize

et al. 2017

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Most terrestrial plants, including crops, engage in beneficial interactions with arbuscular mycorrhizal fungi. Vital to the association is mutual recognition involving the release of diffusible signals into the rhizosphere. Previously, we identified the maize no perception 1 (nope1) mutant to be defective in early signaling. Here, we report cloning of ZmNOPE1 on the basis of synteny with rice. NOPE1 encodes a functional homolog of the Candida albicans N-acetylglucosamine (GlcNAc) transporter NGT1, and represents the first plasma membrane GlcNAc transporter identified from plants. In C. albicans, exposure to GlcNAc activates cell signaling and virulence. Similarly, in Rhizophagus irregularis treatment with rice wild type but not nope1 root exudates induced transcriptome changes associated with signaling function, suggesting a requirement of NOPE1 function for presymbiotic fungal reprogramming.

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“…In at least two lineages, regulation of acetate metabolism is critical for the development and stability of their interactions with host organisms. In Vibrio fischeri, the bioluminescent symbiont of the Hawaiian bobtail squid, Euprymna scolopes, Acs promotes colonization of the juvenile squid (14,15). In Vibrio cholerae, the human pathogen responsible for historical and ongoing global cholera pandemics, Acs is required for virulence in a Drosophila melanogaster model of infection (16).…”

Section: Importancementioning

confidence: 99%

A Putative Acetylation System in Vibrio cholerae Modulates Virulence in Arthropod Hosts

Liimatta

Flaherty

et al. 2018

Appl Environ Microbiol

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Acetylation is a broadly conserved mechanism of covalently modifying the proteome to precisely control protein activity. In bacteria, central metabolic enzymes and regulatory proteins, including those involved in virulence, can be targeted for acetylation. In this study, we directly link a putative acetylation system to metabolite-dependent virulence in the pathogen We demonstrate that the and genes, which encode homologs of a deacetylase and an acetyltransferase, respectively, modulate metabolism of acetate, a bacterially derived short-chain fatty acid with important physiological roles in a diversity of host organisms. In , a model arthropod host for infection, the pathogen consumes acetate within the gastrointestinal tract, which contributes to fly mortality. We show that deletion of impairs growth on acetate minimal medium, delays the consumption of acetate from rich medium, and reduces virulence of toward These impacts can be reversed by complementing or by introducing a deletion of into the Δ background. We further show that controls the accumulation of triglycerides in the midgut, which suggests that directly modulates metabolite levels In K-12, is upregulated by cAMP-cAMP receptor protein (CRP), and we identified a similar pattern of regulation in , arguing that the system is activated in response to similar environmental cues. In summary, we demonstrate that proteins likely involved in acetylation can modulate the outcome of infection by regulating metabolite exchange between pathogens and their colonized hosts. The bacterium causes severe disease in humans, and strains can persist in the environment in association with a wide diversity of host species. By investigating the molecular mechanisms that underlie these interactions, we can better understand constraints affecting the ecology and evolution of this global pathogen. The model of infection has revealed that bacterial regulation of acetate and other small metabolites from within the fly gastrointestinal tract is crucial for its virulence. Here, we demonstrate that genes that may modify the proteome of affect virulence toward , most likely by modulating central metabolic pathways that control the consumption of acetate as well as other small molecules. These findings further highlight the many layers of regulation that tune bacterial metabolism to alter the trajectory of interactions between bacteria and their hosts.

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A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

Cited by 18 publications

References 52 publications

Transcriptional characterization of Vibrio fischeri during colonization of juvenile Euprymna scolopes

Transcriptional characterization of Vibrio fischeri during colonization of juvenile Euprymna scolopes

An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize

A Putative Acetylation System in Vibrio cholerae Modulates Virulence in Arthropod Hosts

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