Type VI secretion system regulation as a consequence of evolutionary pressure

Miyata, Sarah T.; Bachmann, Verena; Pukatzki, Stefan

doi:10.1099/jmm.0.053983-0

Cited by 62 publications

(67 citation statements)

References 123 publications

(278 reference statements)

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“…Nevertheless, T6SSs are widespread in nature and not confined to known pathogens (Costa et al, 2015). In some cases, T6SSs can kill prokaryotic cells as well (Miyata et al, 2013). A recent pyrosequencing study of the protistan community in T. swinhoei revealed the existence of radiolarians, which might prey on symbiotic prokaryotes (He et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

Liu

Gao

et al. 2016

Front. Microbiol.

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“Entotheonella” (phylum “Tectomicrobia”) is a filamentous symbiont that produces almost all known bioactive compounds derived from the Lithistida sponge Theonella swinhoei. In contrast to the comprehensive knowledge of its secondary metabolism, knowledge of its lifestyle, resilience, and interaction with the sponge host and other symbionts remains rudimentary. In this study, we obtained two “Entotheonella” genomes from T. swinhoei from the South China Sea through metagenome binning, and used a RASTtk pipeline to achieve better genome annotation. The high average nucleotide index values suggested they were the same phylotypes as the two “Entotheonella” phylotypes from T. swinhoei from the Japan Sea. Genomic features related to utilization of various carbon sources, peptidase secretion, CO2 fixation, sulfate reduction, anaerobic respiration, and denitrification indicated the mixotrophic nature of “Entotheonella.” The endospore-forming potential along with metal- and antibiotic resistance indicated “Entotheonella” was highly resilient to harsh conditions. The potential for endospore formation also explained the widespread distribution of “Entotheonella” to some extent. The discovery of Type II (general secretion pathway proteins and the Widespread Colonization Island) and Type VI secretion systems in “Entotheonella” suggested it could secrete extracellular hydrolases, form tight adhesion, act against phagocytes, and kill other prokaryotes. Overall, the newly discovered genomic features suggest “Entotheonella” is a highly competitive member of the symbiotic community of T. swinhoei.

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Section: Resultsmentioning

confidence: 99%

New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

Liu

Gao

et al. 2016

Front. Microbiol.

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“…The type V secretion system forms a pore in the outer membrane through which the passenger domain passes to the cell surface (280,281). The newly identified type VI secretion system is a complex bacterial export pathway composed of at least two complexes, a dynamic bacteriophage-like structure and a cell envelope-spanning membrane-associated assembly (282,283). Like the type III and IV secretion systems, the type VI secretion system translocates substrates directly into recipient cells in a contact-dependent manner.…”

Section: Mechanisms Of Pathogenesis Of Human Enterovirulent Bacteriamentioning

confidence: 99%

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Moal

Servin

2013

Microbiol Mol Biol Rev

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SUMMARY Hosts are protected from attack by potentially harmful enteric microorganisms, viruses, and parasites by the polarized fully differentiated epithelial cells that make up the epithelium, providing a physical and functional barrier. Enterovirulent bacteria interact with the epithelial polarized cells lining the intestinal barrier, and some invade the cells. A better understanding of the cross talk between enterovirulent bacteria and the polarized intestinal cells has resulted in the identification of essential enterovirulent bacterial structures and virulence gene products playing pivotal roles in pathogenesis. Cultured animal cell lines and cultured human nonintestinal, undifferentiated epithelial cells have been extensively used for understanding the mechanisms by which some human enterovirulent bacteria induce intestinal disorders. Human colon carcinoma cell lines which are able to express in culture the functional and structural characteristics of mature enterocytes and goblet cells have been established, mimicking structurally and functionally an intestinal epithelial barrier. Moreover, Caco-2-derived M-like cells have been established, mimicking the bacterial capture property of M cells of Peyer's patches. This review intends to analyze the cellular and molecular mechanisms of pathogenesis of human enterovirulent bacteria observed in infected cultured human colon carcinoma enterocyte-like HT-29 subpopulations, enterocyte-like Caco-2 and clone cells, the colonic T84 cell line, HT-29 mucus-secreting cell subpopulations, and Caco-2-derived M-like cells, including cell association, cell entry, intracellular lifestyle, structural lesions at the brush border, functional lesions in enterocytes and goblet cells, functional and structural lesions at the junctional domain, and host cellular defense responses.

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“…Previous studies have highlighted that T6SS gene clusters are tightly regulated (38)(39)(40). The S. Typhimurium SPI-6 T6SS gene cluster is repressed by the DNA-binding protein H-NS and thus limits its antibacterial activity (36).…”

Section: S Typhimurium T6ss Kills Microbiota Members and Is Enhanced Bymentioning

confidence: 99%

Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut

Sana

Flaugnatti

Lugo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

303

292

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The mammalian gastrointestinal tract is colonized by a high-density polymicrobial community where bacteria compete for niches and resources. One key competition strategy includes cell contact-dependent mechanisms of interbacterial antagonism, such as the type VI secretion system (T6SS), a multiprotein needle-like apparatus that injects effector proteins into prokaryotic and/or eukaryotic target cells. However, the contribution of T6SS antibacterial activity during pathogen invasion of the gut has not been demonstrated. We report that successful establishment in the gut by the enteropathogenic bacterium Salmonella enterica serovar Typhimurium requires a T6SS encoded within Salmonella pathogenicity island-6 (SPI-6). In an in vitro setting, we demonstrate that bile salts increase SPI-6 antibacterial activity and that S. Typhimurium kills commensal bacteria in a T6SS-dependent manner. Furthermore, we provide evidence that one of the two T6SS nanotube subunits, Hcp1, is required for killing Klebsiella oxytoca in vitro and that this activity is mediated by the specific interaction of Hcp1 with the antibacterial amidase Tae4. Finally, we show that K. oxytoca is killed in the host gut in an Hcp1-dependent manner and that the T6SS antibacterial activity is essential for Salmonella to establish infection within the host gut. Our findings provide an example of pathogen T6SS-dependent killing of commensal bacteria as a mechanism to successfully colonize the host gut.

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Type VI secretion system regulation as a consequence of evolutionary pressure

Cited by 62 publications

References 123 publications

New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut

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