DOI: 10.1128/iai.68.8.4598-4603.2000. Switching of Flagellar Motility in <i>Helicobacter pylori</i> by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in <i>fliP</i> , a Gene Encoding a Basal Body Protein

Switching of Flagellar Motility in Helicobacter pylori by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in fliP , a Gene Encoding a Basal Body Protein

10.1128/iai.68.8.4598-4603.2000

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACT The genome of Helicobacter pylori contains numerous simple nucleotide repeats that have been proposed to have regulatory functions and to compensate for the conspicuous dearth of master regulatory pathways in this highly host-adapted bacterium. H. pylori strain 26695, whose genomic sequence was determined by The Institute for Genomic Research (TIGR), contains a repeat of nine cytidines in the fliP flagellar basal body gene that splits the open reading frame in two parts. In this work, we demonstrate that the 26695 C9 strain with a split fliP gene as sequenced by TIGR was nonflagellated and nonmotile. In contrast, earlier isolates of strain 26695 selected by positive motility testing as well as pig-passaged derivatives of 26695 were all flagellated and highly motile. All of these motile strains had a C 8 repeat and consequently a contiguous fliP reading frame. By screening approximately 50,000 colonies of 26695 C9 for motility in soft agar, a motile revertant with a C 8 repeat could be isolated, proving that the described switch is reversible. The fliP genes of 20 motile clinical H. pylori isolates from different geographic regions possessed intact fliP genes with repeats of eight cytidines or the sequence CCCCACCC in its place. Isogenic fliP mutants of a motile, C 8 repeat isolate of strain 26695 were constructed by allelic exchange mutagenesis and found to be defective in flagellum biogenesis. Mutants produced only small amounts of flagellins, while the transcription of flagellin genes appeared unchanged. These results strongly suggest a unique mechanism regulating motility in H. pylori which relies on slipped-strand mispairing-mediated mutagenesis of fliP .

Bibliography

Josenhans, C., Eaton, K. A., Thevenot, T., & Suerbaum, S. (2000). Switching of Flagellar Motility in Helicobacter pylori by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in fliP , a Gene Encoding a Basal Body Protein. Infection and Immunity, 68(8), 4598â4603.

Authors 4

Christine Josenhans (first)
Kathryn A. Eaton (additional)
Tracy Thevenot (additional)
Sebastian Suerbaum (additional)

References 40 Referenced 85

10.1046/j.1365-2958.1999.01382.x
10.1038/16495
10.1128/iai.65.5.1962-1966.1997
10.1128/IAI.67.10.5361-5366.1999
10.1016/S1097-2765(00)80471-2
10.1128/iai.65.5.1949-1952.1997
10.1128/iai.57.4.1119-1125.1989
10.1099/00222615-37-2-123
10.1128/iai.64.7.2445-2448.1996
10.1046/j.1365-2958.1997.6412010.x
10.1128/jb.174.13.4212-4217.1992
10.1128/jcm.27.3.436-441.1989
10.1002/j.1460-2075.1996.tb00347.x
10.1093/infdis/153.4.658
10.1146/annurev.micro.52.1.231
10.1046/j.1365-2958.1999.01478.x
10.1128/jb.177.11.3010-3020.1995
10.1136/jcp.51.8.623
10.1128/jb.173.3.937-946.1991
10.1128/jb.173.6.1920-1931.1991
10.1016/S0016-5085(97)70155-0
10.1099/00222615-26-2-93
10.1128/jb.176.23.7345-7351.1994
10.1128/jb.176.1.189-197.1994
10.1016/0923-2508(91)90086-P
10.1093/oxfordjournals.molbev.a025960
10.1128/JB.181.5.1388-1394.1999
10.1111/j.1365-2958.1994.tb01307.x
10.1128/JB.182.1.207-210.2000
Sambrook J. Fritsch E. F. Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y
10.1046/j.1365-2958.1998.00768.x
10.1128/jb.179.4.987-997.1997
10.1128/JB.181.2.593-599.1999
10.1128/jb.175.11.3278-3288.1993
10.1073/pnas.95.21.12619
10.1038/41483
10.1002/j.1460-2075.1985.tb04120.x
10.1128/MMBR.62.2.275-293.1998
10.1016/0092-8674(93)90647-9
10.1046/j.1365-2958.1999.01268.x

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 5:58 a.m.)
Deposited	3 years, 5 months ago (March 4, 2022, 8:41 p.m.)
Indexed	5 months, 1 week ago (March 19, 2025, 12:24 p.m.)
Issued	25 years ago (Aug. 1, 2000)
Published	25 years ago (Aug. 1, 2000)
Published Print	25 years ago (Aug. 1, 2000)

Funders 0

None

BibTeX

@article{Josenhans_2000, title={Switching of Flagellar Motility in Helicobacter pylori by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in fliP , a Gene Encoding a Basal Body Protein}, volume={68}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.68.8.4598-4603.2000}, DOI={10.1128/iai.68.8.4598-4603.2000}, number={8}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Josenhans, Christine and Eaton, Kathryn A. and Thevenot, Tracy and Suerbaum, Sebastian}, editor={Barbieri, J. T.}, year={2000}, month=aug, pages={4598–4603} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        3,
        19
      ]
    ],
    "date-time": "2025-03-19T16:24:44Z",
    "timestamp": 1742401484211
  },
  "reference-count": 40,
  "publisher": "American Society for Microbiology",
  "issue": "8",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2000,
            8,
            1
          ]
        ],
        "date-time": "2000-08-01T00:00:00Z",
        "timestamp": 965088000000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        8
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            The genome of\n            <jats:italic>Helicobacter pylori</jats:italic>\n            contains numerous simple nucleotide repeats that have been proposed to have regulatory functions and to compensate for the conspicuous dearth of master regulatory pathways in this highly host-adapted bacterium.\n            <jats:italic>H. pylori</jats:italic>\n            strain 26695, whose genomic sequence was determined by The Institute for Genomic Research (TIGR), contains a repeat of nine cytidines in the\n            <jats:italic>fliP</jats:italic>\n            flagellar basal body gene that splits the open reading frame in two parts. In this work, we demonstrate that the 26695\n            <jats:sub>C9</jats:sub>\n            strain with a split\n            <jats:italic>fliP</jats:italic>\n            gene as sequenced by TIGR was nonflagellated and nonmotile. In contrast, earlier isolates of strain 26695 selected by positive motility testing as well as pig-passaged derivatives of 26695 were all flagellated and highly motile. All of these motile strains had a C\n            <jats:sub>8</jats:sub>\n            repeat and consequently a contiguous\n            <jats:italic>fliP</jats:italic>\n            reading frame. By screening approximately 50,000 colonies of 26695\n            <jats:sub>C9</jats:sub>\n            for motility in soft agar, a motile revertant with a C\n            <jats:sub>8</jats:sub>\n            repeat could be isolated, proving that the described switch is reversible. The\n            <jats:italic>fliP</jats:italic>\n            genes of 20 motile clinical\n            <jats:italic>H. pylori</jats:italic>\n            isolates from different geographic regions possessed intact\n            <jats:italic>fliP</jats:italic>\n            genes with repeats of eight cytidines or the sequence CCCCACCC in its place. Isogenic\n            <jats:italic>fliP</jats:italic>\n            mutants of a motile, C\n            <jats:sub>8</jats:sub>\n            repeat isolate of strain 26695 were constructed by allelic exchange mutagenesis and found to be defective in flagellum biogenesis. Mutants produced only small amounts of flagellins, while the transcription of flagellin genes appeared unchanged. These results strongly suggest a unique mechanism regulating motility in\n            <jats:italic>H. pylori</jats:italic>\n            which relies on slipped-strand mispairing-mediated mutagenesis of\n            <jats:italic>fliP</jats:italic>\n            .\n          </jats:p>",
  "DOI": "10.1128/iai.68.8.4598-4603.2000",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T09:58:35Z",
    "timestamp": 1027763915000
  },
  "page": "4598-4603",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 85,
  "title": "Switching of Flagellar Motility in\n            <i>Helicobacter pylori</i>\n            by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in\n            <i>fliP</i>\n            , a Gene Encoding a Basal Body Protein",
  "prefix": "10.1128",
  "volume": "68",
  "author": [
    {
      "given": "Christine",
      "family": "Josenhans",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Institute of Hygiene and Microbiology, University of Wu\u0308rzburg, D-97080 Wu\u0308rzburg,1 and"
        },
        {
          "name": "<!--label omitted: 2-->Department of Medical Microbiology, Ruhr-Universita\u0308t Bochum, D-44780 Bochum,2 Germany, and"
        }
      ]
    },
    {
      "given": "Kathryn A.",
      "family": "Eaton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 3-->Department of Veterinary Biosciences, Ohio State University, Columbus, Ohio3"
        }
      ]
    },
    {
      "given": "Tracy",
      "family": "Thevenot",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 3-->Department of Veterinary Biosciences, Ohio State University, Columbus, Ohio3"
        }
      ]
    },
    {
      "given": "Sebastian",
      "family": "Suerbaum",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Institute of Hygiene and Microbiology, University of Wu\u0308rzburg, D-97080 Wu\u0308rzburg,1 and"
        },
        {
          "name": "<!--label omitted: 2-->Department of Medical Microbiology, Ruhr-Universita\u0308t Bochum, D-44780 Bochum,2 Germany, and"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1999.01382.x"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/16495"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.5.1962-1966.1997"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.67.10.5361-5366.1999"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(00)80471-2"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.5.1949-1952.1997"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.57.4.1119-1125.1989"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00222615-37-2-123"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.7.2445-2448.1996"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.6412010.x"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.174.13.4212-4217.1992"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.27.3.436-441.1989"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1996.tb00347.x"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/153.4.658"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.micro.52.1.231"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1999.01478.x"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.177.11.3010-3020.1995"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1136/jcp.51.8.623"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.173.3.937-946.1991"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.173.6.1920-1931.1991"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0016-5085(97)70155-0"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00222615-26-2-93"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.176.23.7345-7351.1994"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.176.1.189-197.1994"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0923-2508(91)90086-P"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/oxfordjournals.molbev.a025960"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.5.1388-1394.1999"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1994.tb01307.x"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.182.1.207-210.2000"
    },
    {
      "key": "e_1_3_2_31_2",
      "unstructured": "Sambrook\nJ.\nFritsch\nE. F.\nManiatis\nT.\nMolecular cloning: a laboratory manual\n2nd ed.\n1989\nCold Spring Harbor Laboratory Press\nCold Spring Harbor N.Y"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.00768.x"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.4.987-997.1997"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.2.593-599.1999"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.175.11.3278-3288.1993"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.21.12619"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/41483"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1985.tb04120.x"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MMBR.62.2.275-293.1998"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90647-9"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1999.01268.x"
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.68.8.4598-4603.2000",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.68.8.4598-4603.2000",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        3,
        5
      ]
    ],
    "date-time": "2022-03-05T01:41:42Z",
    "timestamp": 1646444502000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.68.8.4598-4603.2000"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "J. T.",
      "family": "Barbieri",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        8
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2000,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.68.8.4598-4603.2000"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.68.8.4598-4603.2000",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        2000,
        8
      ]
    ]
  },
  "assertion": [
    {
      "value": "2000-01-28",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2000-05-15",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2000-08-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}