DOI: 10.1073/pnas.1012931107. The <i>Vibrio cholerae</i> type VI secretion system displays antimicrobial properties

The Vibrio cholerae type VI secretion system displays antimicrobial properties

10.1073/pnas.1012931107

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The acute diarrheal disease cholera is caused by the marine bacterium Vibrio cholerae . A type VI secretion system (T6SS), which is structurally similar to the bacteriophage cell-puncturing device, has been recently identified in V. cholerae and is used by this organism to confer virulence toward phagocytic eukaryotes, such as J774 murine macrophages and Dictyostelium discoideum . We tested the interbacterial virulence of V. cholerae strain V52, an O37 serogroup with a constitutively active T6SS. V52 was found to be highly virulent toward multiple Gram-negative bacteria, including Escherichia coli and Salmonella Typhimurium, and caused up to a 100,000-fold reduction in E. coli survival. Because the T6SS-deficient mutants V52Δ vasK and V52Δ vasH showed toxicity defects that could be complemented, virulence displayed by V. cholerae depends on a functional T6SS. V. cholerae V52 and strains of the O1 serogroup were resistant to V52, suggesting that V. cholerae has acquired immunity independently of its serogroup. We hypothesize that the T6SS, in addition to targeting eukaryotic host cells, confers toxicity toward other bacteria, providing a means of interspecies competition to enhance environmental survival. Thus, the V. cholerae T6SS may enhance the survival of V. cholerae in its aquatic ecosystem during the transmission of cholera and between epidemics.

Bibliography

MacIntyre, D. L., Miyata, S. T., Kitaoka, M., & Pukatzki, S. (2010). The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proceedings of the National Academy of Sciences, 107(45), 19520â19524.

Authors 4

Dana L. MacIntyre (first)
Sarah T. Miyata (additional)
Maya Kitaoka (additional)
Stefan Pukatzki (additional)

References 24 Referenced 385

10.1016/S0140-6736(05)71877-8
M Kosek, C Bern, RL Guerrant, The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81, 197–204 (2003). / Bull World Health Organ / The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000 by Kosek M (2003)
10.1073/pnas.0510322103
10.1186/1471-2164-10-104
10.1016/j.chom.2009.12.007
10.1371/journal.ppat.1001068
10.1073/pnas.0813360106
10.1073/pnas.0706532104
10.1016/j.mib.2008.11.010
10.1073/pnas.0712247105
10.1073/pnas.0900044106
MS Islam, BS Drasar, RB Sack, The aquatic flora and fauna as reservoirs of Vibrio cholerae: A review. J Diarrhoeal Dis Res 12, 87–96 (1994). / J Diarrhoeal Dis Res / The aquatic flora and fauna as reservoirs of Vibrio cholerae: A review by Islam MS (1994)
10.1128/aem.45.1.275-283.1983
10.1172/JCI106874
10.1128/iai.1.3.293-299.1970
10.1016/j.chom.2009.02.005
10.1038/35092500
10.1111/j.1462-2920.2009.02005.x
10.1128/JB.00945-08
10.1186/1471-2164-10-354
10.1016/S0300-9084(02)01422-0
JD Oliver, The viable but nonculturable state in bacteria. J Microbiol 43, 93–100 (2005). / J Microbiol / The viable but nonculturable state in bacteria by Oliver JD (2005)
10.1038/nrmicro2259
10.1038/nbt1037

Dates

Type	When
Created	14 years, 10 months ago (Oct. 26, 2010, 12:46 a.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 8:13 p.m.)
Indexed	1 week ago (Aug. 26, 2025, 2:23 a.m.)
Issued	14 years, 10 months ago (Oct. 25, 2010)
Published	14 years, 10 months ago (Oct. 25, 2010)
Published Online	14 years, 10 months ago (Oct. 25, 2010)
Published Print	14 years, 9 months ago (Nov. 9, 2010)

Funders 0

None

BibTeX

@article{MacIntyre_2010, title={The Vibrio cholerae type VI secretion system displays antimicrobial properties}, volume={107}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1012931107}, DOI={10.1073/pnas.1012931107}, number={45}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={MacIntyre, Dana L. and Miyata, Sarah T. and Kitaoka, Maya and Pukatzki, Stefan}, year={2010}, month=oct, pages={19520–19524} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        26
      ]
    ],
    "date-time": "2025-08-26T06:23:22Z",
    "timestamp": 1756189402325
  },
  "reference-count": 24,
  "publisher": "Proceedings of the National Academy of Sciences",
  "issue": "45",
  "content-domain": {
    "domain": [
      "www.pnas.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2010,
        11,
        9
      ]
    ]
  },
  "abstract": "<jats:p>\n            The acute diarrheal disease cholera is caused by the marine bacterium\n            <jats:italic>Vibrio cholerae</jats:italic>\n            . A type VI secretion system (T6SS), which is structurally similar to the bacteriophage cell-puncturing device, has been recently identified in\n            <jats:italic>V. cholerae</jats:italic>\n            and is used by this organism to confer virulence toward phagocytic eukaryotes, such as J774 murine macrophages and\n            <jats:italic>Dictyostelium discoideum</jats:italic>\n            . We tested the interbacterial virulence of\n            <jats:italic>V. cholerae</jats:italic>\n            strain V52, an O37 serogroup with a constitutively active T6SS. V52 was found to be highly virulent toward multiple Gram-negative bacteria, including\n            <jats:italic>Escherichia coli</jats:italic>\n            and\n            <jats:italic>Salmonella</jats:italic>\n            Typhimurium, and caused up to a 100,000-fold reduction in\n            <jats:italic>E. coli</jats:italic>\n            survival. Because the T6SS-deficient mutants V52\u0394\n            <jats:italic>vasK</jats:italic>\n            and V52\u0394\n            <jats:italic>vasH</jats:italic>\n            showed toxicity defects that could be complemented, virulence displayed by\n            <jats:italic>V. cholerae</jats:italic>\n            depends on a functional T6SS.\n            <jats:italic>V. cholerae</jats:italic>\n            V52 and strains of the O1 serogroup were resistant to V52, suggesting that\n            <jats:italic>V. cholerae</jats:italic>\n            has acquired immunity independently of its serogroup. We hypothesize that the T6SS, in addition to targeting eukaryotic host cells, confers toxicity toward other bacteria, providing a means of interspecies competition to enhance environmental survival. Thus, the\n            <jats:italic>V. cholerae</jats:italic>\n            T6SS may enhance the survival of\n            <jats:italic>V. cholerae</jats:italic>\n            in its aquatic ecosystem during the transmission of cholera and between epidemics.\n          </jats:p>",
  "DOI": "10.1073/pnas.1012931107",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2010,
        10,
        26
      ]
    ],
    "date-time": "2010-10-26T04:46:40Z",
    "timestamp": 1288068400000
  },
  "page": "19520-19524",
  "update-policy": "http://dx.doi.org/10.1073/pnas.cm10313",
  "source": "Crossref",
  "is-referenced-by-count": 385,
  "title": "The\n            <i>Vibrio cholerae</i>\n            type VI secretion system displays antimicrobial properties",
  "prefix": "10.1073",
  "volume": "107",
  "author": [
    {
      "given": "Dana L.",
      "family": "MacIntyre",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada T6G 2H7"
        }
      ]
    },
    {
      "given": "Sarah T.",
      "family": "Miyata",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada T6G 2H7"
        }
      ]
    },
    {
      "given": "Maya",
      "family": "Kitaoka",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada T6G 2H7"
        }
      ]
    },
    {
      "given": "Stefan",
      "family": "Pukatzki",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada T6G 2H7"
        }
      ]
    }
  ],
  "member": "341",
  "published-online": {
    "date-parts": [
      [
        2010,
        10,
        25
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_3_3_1_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0140-6736(05)71877-8"
    },
    {
      "key": "e_1_3_3_2_2",
      "first-page": "197",
      "article-title": "The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000",
      "volume": "81",
      "author": "Kosek M",
      "year": "2003",
      "unstructured": "M Kosek, C Bern, RL Guerrant, The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81, 197\u2013204 (2003).",
      "journal-title": "Bull World Health Organ"
    },
    {
      "key": "e_1_3_3_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0510322103"
    },
    {
      "key": "e_1_3_3_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2164-10-104"
    },
    {
      "key": "e_1_3_3_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.chom.2009.12.007"
    },
    {
      "key": "e_1_3_3_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.ppat.1001068"
    },
    {
      "key": "e_1_3_3_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0813360106"
    },
    {
      "key": "e_1_3_3_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0706532104"
    },
    {
      "key": "e_1_3_3_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.mib.2008.11.010"
    },
    {
      "key": "e_1_3_3_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0712247105"
    },
    {
      "key": "e_1_3_3_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0900044106"
    },
    {
      "key": "e_1_3_3_12_2",
      "first-page": "87",
      "article-title": "The aquatic flora and fauna as reservoirs of Vibrio cholerae: A review",
      "volume": "12",
      "author": "Islam MS",
      "year": "1994",
      "unstructured": "MS Islam, BS Drasar, RB Sack, The aquatic flora and fauna as reservoirs of Vibrio cholerae: A review. J Diarrhoeal Dis Res 12, 87\u201396 (1994).",
      "journal-title": "J Diarrhoeal Dis Res"
    },
    {
      "key": "e_1_3_3_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/aem.45.1.275-283.1983"
    },
    {
      "key": "e_1_3_3_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI106874"
    },
    {
      "key": "e_1_3_3_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.1.3.293-299.1970"
    },
    {
      "key": "e_1_3_3_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.chom.2009.02.005"
    },
    {
      "key": "e_1_3_3_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/35092500"
    },
    {
      "key": "e_1_3_3_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1462-2920.2009.02005.x"
    },
    {
      "key": "e_1_3_3_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.00945-08"
    },
    {
      "key": "e_1_3_3_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2164-10-354"
    },
    {
      "key": "e_1_3_3_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0300-9084(02)01422-0"
    },
    {
      "key": "e_1_3_3_22_2",
      "first-page": "93",
      "article-title": "The viable but nonculturable state in bacteria",
      "volume": "43",
      "author": "Oliver JD",
      "year": "2005",
      "unstructured": "JD Oliver, The viable but nonculturable state in bacteria. J Microbiol 43, 93\u2013100 (2005).",
      "journal-title": "J Microbiol"
    },
    {
      "key": "e_1_3_3_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nrmicro2259"
    },
    {
      "key": "e_1_3_3_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nbt1037"
    }
  ],
  "container-title": "Proceedings of the National Academy of Sciences",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://pnas.org/doi/pdf/10.1073/pnas.1012931107",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        4,
        13
      ]
    ],
    "date-time": "2022-04-13T00:13:08Z",
    "timestamp": 1649808788000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://pnas.org/doi/full/10.1073/pnas.1012931107"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2010,
        10,
        25
      ]
    ]
  },
  "references-count": 24,
  "journal-issue": {
    "issue": "45",
    "published-print": {
      "date-parts": [
        [
          2010,
          11,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1073/pnas.1012931107"
  ],
  "URL": "http://dx.doi.org/10.1073/pnas.1012931107",
  "relation": {},
  "ISSN": [
    "0027-8424",
    "1091-6490"
  ],
  "subject": [],
  "container-title-short": "Proc. Natl. Acad. Sci. U.S.A.",
  "published": {
    "date-parts": [
      [
        2010,
        10,
        25
      ]
    ]
  },
  "assertion": [
    {
      "value": "2010-10-25",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}