Shigella sonnei Encodes a Functional T6SS Used for Interbacterial Competition and Niche Occupancy

Anderson, Mark; Vonaesch, Pascale; Saffarian, Azadeh; Marteyn, Benoît; Sansonetti, Philippe J.

doi:10.1016/j.chom.2017.05.004

Cited by 142 publications

(136 citation statements)

References 43 publications

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“…Additional work demonstrated that T6S contributes to the fitness of Bacteroides fragilis in competition with other bacteria in vitro and in gnotobiotic mice (Chatzidaki-Livanis et al, 2016; Hecht et al, 2016; Russell et al, 2014b; Wexler et al, 2016). These and other data show that the mammalian GI tract is physically conducive to T6SS-dependent interbacterial antagonism, suggesting a potential impact of this pathway on the composition of the human gut microbiome (Anderson et al, 2017; Sana et al, 2016). Here, we sought to define the distribution of the Bacteroidales T6SS and to explore its function in the human gut microbiome through the analysis of several publicly available metagenomic datasets.…”

Section: Introductionsupporting

confidence: 57%

The Landscape of Type VI Secretion across Human Gut Microbiomes Reveals Its Role in Community Composition

Verster

Ross

Radey

et al. 2017

Cell Host & Microbe

145

133

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Summary Although gut microbiome composition is well defined, the mechanisms underlying community assembly remain poorly understood. Bacteroidales possess three genetic architectures (GA1–3) of the type VI secretion system (T6SS), an effector delivery pathway that mediates interbacterial competition. Here we define the distribution and role of GA1–3 in the human gut using metagenomic analysis. We find that adult microbiomes harbor limited effector and cognate immunity genes, suggesting selection for compatibility at the species (GA1, GA2) and strain (GA3) levels. Bacteroides fragilis GA3 is known to mediate potent inter-strain competition, and we observe GA3 enrichment among strains colonizing infant microbiomes, suggesting competition early in life. Additionally, GA3 is associated with increased Bacteroides abundance, indicating that this system confers an advantage in Bacteroides-rich ecosystems. Collectively, these analyses uncover the prevalence of T6SS-dependent competition and reveal its potential role in shaping human gut microbial composition.

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Section: Introductionsupporting

confidence: 57%

The Landscape of Type VI Secretion across Human Gut Microbiomes Reveals Its Role in Community Composition

Verster

Ross

Radey

et al. 2017

Cell Host & Microbe

145

133

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“…Through cycles of extension and contraction, this pathway delivers effector proteins from the cytoplasm of a donor bacterium directly into the periplasm or cytoplasm of a recipient bacterium (3,4). Used by both pathogenic and commensal bacteria of eukaryotes, the T6SS mediates a complex interplay of bacterial cell-cell interactions between beneficial and disease-causing bacteria (5)(6)(7)(8)(9).…”

mentioning

confidence: 99%

Diverse NADase effector families mediate interbacterial antagonism via the type VI secretion system

Tang

Bullen

Ahmad

et al. 2018

Journal of Biological Chemistry

100

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The bacterial type VI secretion system (T6SS) mediates antagonistic cell-cell interactions between competing Gram-negative bacteria. In plant-beneficial bacteria, this pathway has been shown to suppress the growth of bacterial pathogens; however, the identification and mode of action of T6SS effector proteins that mediate this protective effect remain poorly defined. Here, we identify two previously uncharacterized effectors required for interbacterial antagonism by the plant commensal bacterium Pseudomonas protegens. Consistent with the established effector-immunity paradigm for antibacterial T6SS substrates, the toxic activities of these effectors are neutralized by adjacently encoded cognate immunity determinants. Although one of these effectors, RhsA, belongs to the family of DNase enzymes, the activity of the other was not apparent from its sequence. To determine the mechanism of toxicity of this latter effector, we determined its 1.3 Å crystal structure in complex with its immunity protein and found that it resembles NAD(P) ؉ -degrading enzymes. In line with this structural similarity, biochemical characterization of this effector, termed Tne2 (Type VI secretion NADase effector family 2), demonstrates that it possesses potent NAD(P) ؉ hydrolase activity. Tne2 is the founding member of a widespread family of interbacterial NADases predicted to transit not only the Gram-negative T6SS but also the Gram-positive type VII secretion system, a pathway recently implicated in interbacterial competition among Firmicutes. Together, this work identifies new T6SS effectors employed by a plant commensal bacterium to antagonize its competitors and broadly implicates NAD(P) ؉ -hydrolyzing enzymes as substrates of interbacterial conflict pathways found in diverse bacterial phyla.

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“…The Salmonella Pathogenicity Island Six encodes a T6SS cluster that contributes to the colonisation of mice and chickens. The T6SS of pathogenic Shigella sonnei is also required to colonise the mouse gut (Anderson, Vonaesch, Saffarian, Marteyn, & Sansonetti, 2017). However, no killing of other Gramnegative bacteria was observed (e.g., Enterobacter cloacae, Escherichia coli, or commensals such as Prevotella copri, Parabacteroides distasonis, and Bifidobacterium longum; Sana et al, 2016).…”

Section: The T6ss Arms Race In the Control Of Gut Microbiota/ Pathomentioning

confidence: 99%

Causalities of war: The connection between type VI secretion system and microbiota

Allsopp

Bernal

Nolan

et al. 2020

Cellular Microbiology

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Microbiota niches have space and/or nutrient restrictions, which has led to the coevolution of cooperation, specialisation, and competition within the population.Different animal and environmental niches contain defined resident microbiota that tend to be stable over time and offer protection against undesired intruders. Yet fluxes can occur, which alter the composition of a bacterial population. In humans, the microbiota are now considered a key contributor to maintenance of health and homeostasis, and its alteration leads to dysbiosis. The bacterial type VI secretion system (T6SS) transports proteins into the environment, directly into host cells or can function as an antibacterial weapon by killing surrounding competitors. Upon contact with neighbouring cells, the T6SS fires, delivering a payload of effector proteins. In the absence of an immunity protein, this results in growth inhibition or death of prey leading to a competitive advantage for the attacker. It is becoming apparent that the T6SS has a role in modulating and shaping the microbiota at multiple levels, which is the focus of this review. Discussed here is the T6SS, its role in competition, key examples of its effect upon the microbiota, and future avenues of research.

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Shigella sonnei Encodes a Functional T6SS Used for Interbacterial Competition and Niche Occupancy

Cited by 142 publications

References 43 publications

The Landscape of Type VI Secretion across Human Gut Microbiomes Reveals Its Role in Community Composition

The Landscape of Type VI Secretion across Human Gut Microbiomes Reveals Its Role in Community Composition

Diverse NADase effector families mediate interbacterial antagonism via the type VI secretion system

Causalities of war: The connection between type VI secretion system and microbiota

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