Escherichia coli killing by epidemiologically successful sublineages of Shigella sonnei is mediated by colicins

De Silva, P. Malaka; Bennett, Rebecca J.; Kuhn, Lauriane; Ngondo, Patryk; Debande, Lorine; Njamkepo, Elisabeth; Ho, Brian; Weill, François-Xavier; Marteyn, Benoît S.; Jenkins, Claire; Baker, Kate S.

doi:10.1016/j.ebiom.2023.104822

Cited by 6 publications

(7 citation statements)

References 66 publications

(78 reference statements)

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“…To conclude, we have experimental evidence validating observations that S. sonnei anti-bacterial activity is associated with colicins rather than the T6SS [ 33 ]. We hypothesise that this anti-bacterial activity is likely one factor that helps S. sonnei establish itself during infection of the human gut by competing with closely related strains for common resources in the nutrient limited colon.…”

Section: Discussionsupporting

confidence: 83%

“…We cannot out that a threshold level of induction is required activity to be observed which we did not reach even with our inducible strains. However, our data is in agreement with a recent computational-based study which indicated the ability of S. sonnei to kill E. coli was strongly associated with colicin genes rather than the T6SS [33].…”

Section: Continuedsupporting

confidence: 93%

“…Given the recent study indicating the ability of S. sonnei to kill E. coli had no association with the T6SS [ 33 ], we decided to investigate the T6SS in more detail. The T6SS gene clusters from a selection of strains were identified and compared: EHEC EDL933 which contains a T6SS closely related to S. sonnei [ 18 ] that has been demonstrated to be functional [ 21 ], S. sonnei 53G (a well-studied isolate of lineage two), SS381 and CIP106347 as the representative isolates from lineage three ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Secreted T6SS effector proteins are genetically encoded with cognate immunity proteins which prevent self-intoxication and toxicity to kin-bacteria [28,29,32]. A recent study investigating the anti-bacterial activity of S. sonnei using bacterial genome wide association studies combined with high throughput phenotyping indicated that the ability of S. sonnei to kill E. coli had no association with the T6SS [33].…”

Section: Introductionmentioning

confidence: 99%

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Shigella sonnei utilises colicins during inter-bacterial competition

Leung,

Matanza,

Roche

et al. 2024

Microbiology

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The mammalian colon is one of the most densely populated habitats currently recognised, with 1011–1013 commensal bacteria per gram of colonic contents. Enteric pathogens must compete with the resident intestinal microbiota to cause infection. Among these enteric pathogens are Shigella species which cause approximately 125 million infections annually, of which over 90 % are caused by Shigella flexneri and Shigella sonnei. Shigella sonnei was previously reported to use a Type VI Secretion System (T6SS) to outcompete E. coli and S. flexneri in in vitro and in vivo experiments. S. sonnei strains have also been reported to harbour colicinogenic plasmids, which are an alternative anti-bacterial mechanism that could provide a competitive advantage against the intestinal microbiota. We sought to determine the contribution of both T6SS and colicins to the anti-bacterial killing activity of S. sonnei. We reveal that whilst the T6SS operon is present in S. sonnei, there is evidence of functional degradation of the system through SNPs, indels and IS within key components of the system. We created strains with synthetically inducible T6SS operons but were still unable to demonstrate anti-bacterial activity of the T6SS. We demonstrate that the anti-bacterial activity observed in our in vitro assays was due to colicin activity. We show that S. sonnei no longer displayed anti-bacterial activity against bacteria that were resistant to colicins, and removal of the colicin plasmid from S. sonnei abrogated anti-bacterial activity of S. sonnei. We propose that the anti-bacterial activity demonstrated by colicins may be sufficient for niche competition by S. sonnei within the gastrointestinal environment.

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Section: Discussionsupporting

confidence: 83%

Section: Continuedsupporting

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Shigella sonnei utilises colicins during inter-bacterial competition

Leung,

Matanza,

Roche

et al. 2024

Microbiology

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“…T6SS-mediated bacterial antagonism can significantly impact the structure and diversity of bacterial populations in vitro [ 6 , 26 ]. Notably, however, T6SS-mediated killing can be orders of magnitude less effective in vivo compared to equivalent competitions in vitro [ 25 , 27 , 28 ] and can be less effective at eliminating competing bacteria than diffusible antibacterial toxins [ 29 , 30 ] or toxic metabolites [ 31 , 32 ]. Despite such limitations in killing potential, the T6SS is still widely conserved and present in isolates of nearly all enteric Gram-negative species [ 33 ].…”

Section: Introductionmentioning

confidence: 99%

Use of zebrafish to identify host responses specific to type VI secretion system mediated interbacterial antagonism

Virgo,

Mostowy,

2024

PLoS Pathog

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Interbacterial competition is known to shape the microbial communities found in the host, however the interplay between this competition and host defense are less clear. Here, we use the zebrafish hindbrain ventricle (HBV) as an in vivo platform to investigate host responses to defined bacterial communities with distinct forms of interbacterial competition. We found that antibacterial activity of the type VI secretion system (T6SS) from both Vibrio cholerae and Acinetobacter baylyi can induce host inflammation and sensitize the host to infection independent of any individual effector. Chemical suppression of inflammation could resolve T6SS-dependent differences in host survival, but the mechanism by which this occurred differed between the two bacterial species. By contrast, colicin-mediated antagonism elicited by an avirulent strain of Shigella sonnei induced a negligible host response despite being a more potent bacterial killer, resulting in no impact on A. baylyi or V. cholerae virulence. Altogether, these results provide insight into how different modes of interbacterial competition in vivo affect the host in distinct ways.

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