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Type VI Secretion Systems and the Gut Microbiota

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  • Authors: Michael J. Coyne1, Laurie E. Comstock2
  • Editors: Maria Sandkvist3, Eric Cascales4, Peter J. Christie5
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    Affiliations: 1: Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115; 2: Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115; 3: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 4: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 5: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0009-2018
  • Received 28 August 2018 Accepted 15 January 2019 Published 01 March 2019
  • Laurie E. Comstock, [email protected]
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  • Abstract:

    The human colonic microbiota is a dense ecosystem comprised of numerous microbes, including bacteria, phage, fungi, archaea, and protozoa, that compete for nutrients and space. Studies are beginning to reveal the antagonistic mechanisms that gut bacteria use to compete with other members of this ecosystem. In the healthy human colon, the majority of the Gram-negative bacteria are of the order . Proteobacteria, such as , are numerically fewer but confer important properties to the host, such as colonization resistance. Several enteric pathogens use type VI secretion systems (T6SSs) to antagonize symbiotic gut , facilitating colonization and disease progression. T6SS loci are also widely distributed in human gut , which includes three predominant genera: , , and . There are three distinct genetic architectures of T6SS loci among the gut , termed GA1, GA2, and GA3. GA1 and GA2 T6SS loci are contained on integrative and conjugative elements and are the first T6SS loci shown to be readily transferred in the human gut between numerous species and families of . In contrast, the GA3 T6SSs are present exclusively in . There are divergent regions in all three T6SS GAs that contain genes encoding effector and immunity proteins, many of which function by unknown mechanisms. To date, only the GA3 T6SSs have been shown to antagonize bacteria, and they target nearly all gut species analyzed. This review delves more deeply into properties of the T6SSs of these human gut bacteria and the ecological outcomes of their synthesis .

  • Citation: Coyne M, Comstock L. 2019. Type VI Secretion Systems and the Gut Microbiota. Microbiol Spectrum 7(2):PSIB-0009-2018. doi:10.1128/microbiolspec.PSIB-0009-2018.

References

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/content/journal/microbiolspec/10.1128/microbiolspec.PSIB-0009-2018
2019-03-01
2019-09-20

Abstract:

The human colonic microbiota is a dense ecosystem comprised of numerous microbes, including bacteria, phage, fungi, archaea, and protozoa, that compete for nutrients and space. Studies are beginning to reveal the antagonistic mechanisms that gut bacteria use to compete with other members of this ecosystem. In the healthy human colon, the majority of the Gram-negative bacteria are of the order . Proteobacteria, such as , are numerically fewer but confer important properties to the host, such as colonization resistance. Several enteric pathogens use type VI secretion systems (T6SSs) to antagonize symbiotic gut , facilitating colonization and disease progression. T6SS loci are also widely distributed in human gut , which includes three predominant genera: , , and . There are three distinct genetic architectures of T6SS loci among the gut , termed GA1, GA2, and GA3. GA1 and GA2 T6SS loci are contained on integrative and conjugative elements and are the first T6SS loci shown to be readily transferred in the human gut between numerous species and families of . In contrast, the GA3 T6SSs are present exclusively in . There are divergent regions in all three T6SS GAs that contain genes encoding effector and immunity proteins, many of which function by unknown mechanisms. To date, only the GA3 T6SSs have been shown to antagonize bacteria, and they target nearly all gut species analyzed. This review delves more deeply into properties of the T6SSs of these human gut bacteria and the ecological outcomes of their synthesis .

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Image of FIGURE 1
FIGURE 1

Open reading frame (ORF) maps of one representative locus of each of the three genetic architectures (GA) of T6SS loci of gut . T6SS loci of GA1 and GA2 are present in diverse species, whereas GA3 T6SS loci are confined to . T6SS loci of a given GA are extremely similar to each other except for the divergent regions noted by lines above the genes, which encode known or putative effector and immunity proteins. The major TssD protein of GA3 is noted, as is the TssD protein of the GA2 loci that have C-terminal extensions likely conferring toxin activity. The ends of the GA1 and GA2 loci have not been precisely determined. ORF maps of ICE containing GA1 and GA2 T6SS loci of two species. The T6SS loci are designated by a line above the map. Genes involved in conjugative transfer ( genes) are colored green ( 15 ). The abundant fecal gut from three different healthy humans (CL02, CL09, and CL03) were analyzed for the presence of T6SSs. Seven species were isolated and sequenced from subject CL02 and from subject CL09. Four of the seven species harbor nearly identical GA1 T6SSs loci within a subject, demonstrating transfer of these ICE between these strains in their gut ( 12 , 15 ). In contrast, of the eight species isolated and sequenced from human subject CL03, two contain GA2 T6SS loci, albeit with different divergent regions. Therefore, these GA2 ICE were not transferred between these species. In addition, one species contains a GA1 T6SS locus and the strain from this individual contains a GA3 T6SS locus ( 15 ). Red, green, and yellow dots represent the GA1, GA2, and GA3 T6SS loci.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0009-2018
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Image of FIGURE 2
FIGURE 2

T6SS-mediated antagonism in the mammalian gut. Three different proteobacterial enteric pathogens, , Typhimurium, and , use T6SSs to target resident gut to overcome colonization resistance and cause disease in animal models ( 32 36 ). In the case of , the lysed organisms initiate innate immune responses that upregulate virulence factors and increase dissemination ( 32 ). GA3 T6SS antagonize nearly all gut species . , strong antagonistic effects are seen between two distinct strains likely due to their localization at the mucosal surface, where they will make frequent contacts. This intraspecies antagonism may lead to the dominance of one strain. was also significantly antagonized by a GA3 T6SS, possibly due to overlapping nutritional niches. In contrast, a significant antagonistic effect by the GA3 T6SS of was not observed when this organism was coinoculated with . These varied effects may be due to the substrate preferences of these species, which may spatially segregate them under normal dietary conditions.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0009-2018
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