Type VI secretion systems of pathogenic and commensal bacteria mediate niche occupancy in the gut

Serapio-Palacios, Antonio; Woodward, Sarah E.; Vogt, Stefanie; Deng, Wanyin; Creus-Cuadros, Anna; Huus, Kelsey E.; Cirstea, Mihai; Gerrie, Madeleine; Barcik, Weronika; Yu, Hongbing; Finlay, B. Brett

doi:10.1016/j.celrep.2022.110731

Cited by 34 publications

(17 citation statements)

References 89 publications

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“…174,175 Gram-negative pathogens commonly encode the secretion system T6SS, which can mediate interbacterial toxicity and enable pathogens to attack the resident microbiota, conferring a competitive advantage. 20,178 Then, instead of killing the competitor strains, T6SS…”

Section: Toxins Delivered By Specialized Secretion Systemsmentioning

confidence: 99%

“…The secretion systems are expressed during colonization and deliver a wide range of effectors to provide an advantage in a dysbiotic gut 174,175 . Gram‐negative pathogens commonly encode the secretion system T6SS, which can mediate interbacterial toxicity and enable pathogens to attack the resident microbiota, conferring a competitive advantage 20,178 . Then, instead of killing the competitor strains, T6SS increases the intestinal movements that lead to the expulsion of some commensals of the gut microbiota 13,179 .…”

Section: Dysbiosis Induced By Pathogensmentioning

confidence: 99%

See 1 more Smart Citation

Fish disease and intestinal microbiota: A close and indivisible relationship

Félix

Garibay-Valdez

Vargas‐Albores

et al. 2022

Reviews in Aquaculture

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The gut microbiota is currently one of the most studied 'organs' in animals, and fish are no exception. A complex diversity of microbes, including bacteria, archaea, yeast and fungus, constitute the gut microbiota, creating a complex interaction with their host and accomplishing multiple beneficial functions, such as food digestion, nutrient absorption, immune system, endocrine and stress response. The microbiotapathogen interaction protects the host by mounting colonization resistance, competing for nutrients and space. Changes in the balance of the microbiota community could affect their structure and homeostasis, inducing dysbiosis. In addition, invading pathogens can induce dysbiosis by evading the host's defence barriers, acquiring nutrients from the fish host, using metabolites produced by the microbiota and producing toxins. In this regard, understanding the interactions within the fish gut microbiota is essential to prevent pathogen establishment in the host. Hence, this review describes the close and indivisible relationships and interactions between gut microbiota and pathogens that could lead to dysbiosis and disease.

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Section: Toxins Delivered By Specialized Secretion Systemsmentioning

confidence: 99%

Section: Dysbiosis Induced By Pathogensmentioning

confidence: 99%

Fish disease and intestinal microbiota: A close and indivisible relationship

Félix

Garibay-Valdez

Vargas‐Albores

et al. 2022

Reviews in Aquaculture

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“… 54 Notably, the T6SS can be used by both pathogenic and commensal bacterial to compete for enteric niches. 55 …”

Section: Modeling Of Enteric Bacterial Infections In Monolayer Culturesmentioning

confidence: 99%

In vitro and ex vivo modeling of enteric bacterial infections

2022

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Enteric bacterial infections contribute substantially to global disease burden and mortality, particularly in the developing world. In vitro 2D monolayer cultures have provided critical insights into the fundamental virulence mechanisms of a multitude of pathogens, including Salmonella enterica serovars Typhimurium and Typhi, Vibrio cholerae, Shigella spp., Escherichia coli and Campylobacter jejuni , which have led to the identification of novel targets for antimicrobial therapy and vaccines. In recent years, the arsenal of experimental systems to study intestinal infections has been expanded by a multitude of more complex models, which have allowed to evaluate the effects of additional physiological and biological parameters on infectivity. Organoids recapitulate the cellular complexity of the human intestinal epithelium while 3D bioengineered scaffolds and microphysiological devices allow to emulate oxygen gradients, flow and peristalsis, as well as the formation and maintenance of stable and physiologically relevant microbial diversity. Additionally, advancements in ex vivo cultures and intravital imaging have opened new possibilities to study the effects of enteric pathogens on fluid secretion, barrier integrity and immune cell surveillance in the intact intestine. This review aims to present a balanced and updated overview of current intestinal in vitro and ex vivo methods for modeling of enteric bacterial infections. We conclude that the different paradigms are complements rather than replacements and their combined use promises to further our understanding of host-microbe interactions and their impacts on intestinal health.

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“…The role of the T6SS in mammalian gut microbiome ecology is an emerging field. T6SS activity during invasion by enteric pathogens, including species of the Shigella, Salmonella, and Citrobacter genera, facilitates colonization and subsequent pathogenesis typically through the eradication of phylogenetically related endogenous symbionts [17][18][19] . In the human gut, the most abundant T6SS-encoding taxon is the order Bacteroidales, including species of the Parabacteroides and Bacteroides genera 20 .…”

Section: Introductionmentioning

confidence: 99%

Community composition and the environment modulate the population dynamics of type VI secretion in human gut bacteria

Robitaille

Simmons

Verster

et al. 2023

Preprint

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Understanding the relationship between the composition of the human gut microbiota and the ecological forces shaping it is of high importance as progress towards therapeutic modulation of the microbiota advances. However, given the inaccessibility of the gastrointestinal tract, our knowledge of the biogeographical and ecological relationships between physically interacting taxa has been limited to date. It has been suggested that interbacterial antagonism plays an important role in gut community dynamics, but in practice the conditions under which antagonistic behavior is favored or disfavored by selection in the gut environment are not well known. Here, using phylogenomics of bacterial isolate genomes and analysis of infant and adult fecal metagenomes, we show that the contact-dependent type VI secretion system (T6SS) is repeatedly lost from the genomes of Bacteroides fragilis in adults compare to infants. Although this result implies a significant fitness cost to the T6SS, but we could not identify in vitro conditions under which such a cost manifests. Strikingly, however, experiments in mice illustrated that the B. fragilis T6SS can be favored or disfavored in the gut environment, depending on the strains and species in the surrounding community and their susceptibility to T6SS antagonism. We use a variety of ecological modeling techniques to explore the possible local community structuring conditions that could underlie the results of our larger scale phylogenomic and mouse gut experimental approaches. The models illustrate robustly that the pattern of local community structuring in space can modulate the extent of interactions between T6SS-producing, sensitive, and resistant bacteria, which in turn control the balance of fitness costs and benefits of performing contact-dependent antagonistic behavior. Taken together, our genomic analyses, in vivo studies, and ecological theory point toward new integrative models for interrogating the evolutionary dynamics of type VI secretion and other predominant modes of antagonistic interaction in diverse microbiomes.

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Type VI secretion systems of pathogenic and commensal bacteria mediate niche occupancy in the gut

Cited by 34 publications

References 89 publications

Fish disease and intestinal microbiota: A close and indivisible relationship

Fish disease and intestinal microbiota: A close and indivisible relationship

In vitro and ex vivo modeling of enteric bacterial infections

Community composition and the environment modulate the population dynamics of type VI secretion in human gut bacteria

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