<i>Salmonella</i> Typhimurium uses anaerobic respiration to overcome propionate-mediated colonization resistance

Cd, Shelton; W, Yoo; Ng, Shealy; Tp, Torres; Jk, Zieba; Mw, Calcutt; Nj, Foegeding; D, Kim; J, Kim; Sungpil, Ryu; Mx, Byndloss

doi:10.1101/2021.05.25.445690

Cited by 3 publications

(2 citation statements)

References 49 publications

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“…The use of tetrathionate and nitrate as terminal electron acceptors allows Salmonella to use poorly fermentable carbon sources such as ethanolamine derived from enterocytes membrane; fructose‐asparagine derived from host diet; and 1,2‐propanediol, succinate, and propionate that are by‐products of microbial fermentation [17,19,93–95]. The exploitation of these carbon sources ensures a growth advantage over commensal bacteria, which solely rely on fermentation for growth [17,19,93–95].…”

Section: Inflammation and The Newly Created Nichementioning

confidence: 99%

Revisiting the steps of Salmonella gut infection with a focus on antagonistic interbacterial interactions

et al. 2021

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A commensal microbial community is established in the mammalian gut during its development, and these organisms protect the host against pathogenic invaders. The hallmark of noninvasive Salmonella gut infection is the induction of inflammation via effector proteins secreted by the type III secretion system, which modulate host responses to create a new niche in which the pathogen can overcome the colonization resistance imposed by the microbiota. Several studies have shown that endogenous microbes are important to control Salmonella infection by competing for resources. However, there is limited information about antimicrobial mechanisms used by commensals and pathogens during these in vivo disputes for niche control. This review aims to revisit the steps that Salmonella needs to overcome during gut colonization—before and after the induction of inflammation—to achieve an effective infection. We focus on a series of reported and hypothetical antagonistic interbacterial interactions in which both contact‐independent and contact‐dependent mechanisms might define the outcome of the infection.

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Section: Inflammation and The Newly Created Nichementioning

confidence: 99%

Revisiting the steps of Salmonella gut infection with a focus on antagonistic interbacterial interactions

et al. 2021

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“…Earlier work showed that Salmonella induced inflammation created reactive oxygen and nitrogen species in the luminal environment, increasing the availability of oxygen and potentiating formation of tetrathionate and nitrate [9]. Increased concentrations of these terminal electron acceptors allowed Salmonella to respire and out-compete obligate fermentative commensals like members of the Clostridia [6,10]. Additionally, in the remodeled gut ecosystem respiring Salmonella benefited from unique access to non-competitive carbon sources like propionate and ethanolamine [11,12].…”

Section: Introductionmentioning

confidence: 99%

Exposing New Taxonomic Variation with Inflammation – A Murine Model-Specific Genome Database for Gut Microbiome Researchers

Leleiwi

Rodríguez-Ramos

Shaffer

et al. 2022

Preprint

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Background The murine CBA/J mouse model widely supports immunology and enteric pathogen research. This model has illuminated Salmonella interactions with the gut microbiome since pathogen proliferation does not require disruptive pretreatment of the native microbiota, nor does it become systemic, thereby representing an analog to gastroenteritis disease progression in humans. Despite the value to broad research communities, microbiota in CBA/J mice are not represented in current murine microbiome genome catalogs. Results Here we present the first microbial and viral genomic catalog of the CBA/J murine gut microbiome. Using fecal microbial communities from untreated and Salmonella-infected, highly inflamed mice, we performed genomic reconstruction to determine the impacts on gut microbiome membership and functional potential. From high depth whole community sequencing (42.4 Gbps/sample), we reconstructed 2,281 bacterial and 4,129 viral draft genomes. Salmonella challenge significantly altered gut membership in CBA/J mice, revealing 30 genera and 98 species that were conditionally rare and unsampled in non-inflamed mice. Additionally, inflamed communities were depleted in microbial genes that modulate host anti-inflammatory pathways and enriched in genes for respiratory energy generation. Our findings suggest decreases in butyrate concentrations during Salmonella infection corresponded to reductions in the relative abundance in members of the Alistipes. Strain-level comparison of CBA/J microbial genomes to prominent murine gut microbiome databases identified newly sampled lineages in this resource, while comparisons to human gut microbiomes extended the host relevance of dominant CBA/J inflammation resistant strains. Conclusions This CBA/J microbiome database provides the first genomic sampling of relevant, uncultivated microorganisms within the gut from this widely used laboratory model. Using this resource, we curated a functional, strain-resolved view on how Salmonella remodels intact murine gut communities, advancing pathobiome understanding beyond inferences from prior amplicon-based approaches. Salmonella-induced inflammation suppressed Alistipes and other dominant members, while rarer commensals like Lactobacillus and Enterococcus endure. The rare and novel species sampled across this inflammation gradient advance the utility of this microbiome resource to benefit the broad research needs of the CBA/J scientific community, and those using murine models for understanding the impact of inflammation on the gut microbiome more generally.

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Exposing new taxonomic variation with inflammation — a murine model-specific genome database for gut microbiome researchers

et al. 2023

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Background The murine CBA/J mouse model widely supports immunology and enteric pathogen research. This model has illuminated Salmonella interactions with the gut microbiome since pathogen proliferation does not require disruptive pretreatment of the native microbiota, nor does it become systemic, thereby representing an analog to gastroenteritis disease progression in humans. Despite the value to broad research communities, microbiota in CBA/J mice are not represented in current murine microbiome genome catalogs. Results Here we present the first microbial and viral genomic catalog of the CBA/J murine gut microbiome. Using fecal microbial communities from untreated and Salmonella-infected, highly inflamed mice, we performed genomic reconstruction to determine the impacts on gut microbiome membership and functional potential. From high depth whole community sequencing (~ 42.4 Gbps/sample), we reconstructed 2281 bacterial and 4516 viral draft genomes. Salmonella challenge significantly altered gut membership in CBA/J mice, revealing 30 genera and 98 species that were conditionally rare and unsampled in non-inflamed mice. Additionally, inflamed communities were depleted in microbial genes that modulate host anti-inflammatory pathways and enriched in genes for respiratory energy generation. Our findings suggest decreases in butyrate concentrations during Salmonella infection corresponded to reductions in the relative abundance in members of the Alistipes. Strain-level comparison of CBA/J microbial genomes to prominent murine gut microbiome databases identified newly sampled lineages in this resource, while comparisons to human gut microbiomes extended the host relevance of dominant CBA/J inflammation-resistant strains. Conclusions This CBA/J microbiome database provides the first genomic sampling of relevant, uncultivated microorganisms within the gut from this widely used laboratory model. Using this resource, we curated a functional, strain-resolved view on how Salmonella remodels intact murine gut communities, advancing pathobiome understanding beyond inferences from prior amplicon-based approaches. Salmonella-induced inflammation suppressed Alistipes and other dominant members, while rarer commensals like Lactobacillus and Enterococcus endure. The rare and novel species sampled across this inflammation gradient advance the utility of this microbiome resource to benefit the broad research needs of the CBA/J scientific community, and those using murine models for understanding the impact of inflammation on the gut microbiome more generally.

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Salmonella Typhimurium uses anaerobic respiration to overcome propionate-mediated colonization resistance

Cited by 3 publications

References 49 publications

Revisiting the steps of Salmonella gut infection with a focus on antagonistic interbacterial interactions

Revisiting the steps of Salmonella gut infection with a focus on antagonistic interbacterial interactions

Exposing New Taxonomic Variation with Inflammation – A Murine Model-Specific Genome Database for Gut Microbiome Researchers

Exposing new taxonomic variation with inflammation — a murine model-specific genome database for gut microbiome researchers

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