DOI: 10.1128/jcm.42.11.5286-5297.2004. Characterization of “ Candidatus Piscichlamydia salmonis” (Order Chlamydiales ), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon ( Salmo salar )

Characterization of “ Candidatus Piscichlamydia salmonis” (Order Chlamydiales ), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon ( Salmo salar )

10.1128/jcm.42.11.5286-5297.2004

Crossref journal-article

American Society for Microbiology

Journal of Clinical Microbiology (235)

Abstract

ABSTRACT To characterize intracellular gram-negative bacteria associated with epitheliocystis in farmed Atlantic salmon ( Salmo salar ), gills with proliferative lesions were collected for histopathology, conventional transmission and immunoelectron microscopy, in situ hybridization, and DNA extraction during epitheliocystis outbreaks in Ireland and Norway in 1999 and 2000, respectively, and compared by ultrastructure and immunoreactivity to nonproliferative gills from Ireland archived in 1995. Genomic DNA from proliferative gills was used to amplify 16S ribosomal DNA (rDNA) for molecular phylogenetic analyses. Epitheliocystis inclusions from proliferative gills possessed variably elongate reticulate bodies, examples of binary fission, and vacuolated and nonvacuolated intermediate bodies, whereas inclusions in nonproliferative gills had typical chlamydial developmental stages plus distinctive head-and-tail cells. Immunogold processing using anti-chlamydial lipopolysaccharide antibody labeled reticulate bodies from proliferative and nonproliferative gills. 16S rDNA amplified directly from Irish (1999) and Norwegian (2000) gill samples demonstrated 99% nucleotide identity, and riboprobes transcribed from cloned near-full-length 16S rDNA amplicons from Norwegian gills hybridized with inclusions in proliferative lesions from Irish (1999) and Norwegian (2000) sections. A 1,487-bp consensus 16S rRNA gene sequence representing the chlamydia-like bacterium (CLB) from proliferative gills had the highest percent nucleotide identity with endosymbionts of Acanthamoeba spp. (order Chlamydiales ). Molecular phylogenetic relationships inferred from 16S rRNA gene sequences using distance and parsimony indicated that the CLB from proliferative gills branched with members of the order Chlamydiales . “ Candidatus Piscichlamydia salmonis” is proposed for the CLB associated with epitheliocystis from proliferative gills of Atlantic salmon, which exhibits developmental stages different from those identified in nonproliferative gills.

Bibliography

Draghi, A., Popov, V. L., Kahl, M. M., Stanton, J. B., Brown, C. C., Tsongalis, G. J., West, A. B., & Frasca, S. (2004). Characterization of â Candidatus Piscichlamydia salmonisâ (Order Chlamydiales ), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon ( Salmo salar ). Journal of Clinical Microbiology, 42(11), 5286â5297.

Authors 8

Andrew Draghi (first)
Vsevolod L. Popov (additional)
Melissa M. Kahl (additional)
James B. Stanton (additional)
Corrie C. Brown (additional)
Gregory J. Tsongalis (additional)
A. Brian West (additional)
Salvatore Frasca (additional)

References 32 Referenced 119

10.1128/aem.63.1.115-121.1997
Avakyan, A. A., and V. L. Popov. 1984. Rickettsiae and chlamydiae: comparative electron microscopic studies. Acta Virol.28:159-173. / Acta Virol. (1984)
10.3354/dao004009
10.1177/030098589803500301
10.3354/dao037061
10.1099/00207713-51-6-2145
10.1128/jb.169.12.5678-5685.1987
10.1099/00207713-47-2-461
10.1099/00207713-49-2-415
10.1111/j.1558-5646.1985.tb00420.x
10.1128/AEM.66.6.2613-2619.2000
10.1128/AEM.64.10.3599-3606.1998
10.1179/his.1994.17.4.313
10.1177/104063879600800206
10.1086/417338
10.1007/BF02219125
10.1099/00221287-146-5-1231
Ito, S., and Y. Rikihisa. 1981. Techniques for electron microscopy of rickettsiae, p. 213-227. In W. Burgdorfer and R. L. Anacker (ed.), Rickettsiae and rickettsial diseases. Academic Press, New York, N.Y. / Rickettsiae and rickettsial diseases (1981)
10.1099/00207713-49-2-815
10.1111/j.1365-2958.1995.mmi_18030391.x
McDowell, E. M., and B. F. Trump. 1976. Histologic fixatives suitable for diagnostic light and electron microscopy. Arch. Pathol. Lab. Med.100:405-406. / Arch. Pathol. Lab. Med. (1976)
10.1577/1548-8667(1998)010<0043:AMSOTE>2.0.CO;2
Palumbi, S. R. 1996. Nucleic acids II: the polymerase chain reaction, p. 205-248. In D. M. Hillis, C. Moritz, and B. K. Mable (ed.), Molecular systematics, 2nd ed. Sinauer Associates, Inc., Sunderland, Mass. / Molecular systematics (1996)
10.1099/00207713-47-4-1145
10.1016/0044-8486(77)90018-7
10.1128/jb.179.13.4195-4205.1997
Relman, D. A. 1993. Universal bacterial 16S rDNA amplification and sequencing, p. 489-495. In D. H. Pershing, T. F. Smith, F. C. Tenover, and T. J. White (ed.), Diagnostic molecular microbiology: principles and applications. American Society for Microbiology, Washington, D.C. / Diagnostic molecular microbiology: principles and applications (1993)
10.1111/j.1365-2761.1984.tb00935.x
Sheehan D. Z. and B. B. Hrapchak. 1980. Theory and practice of histotechnology. Bettelle Press Columbus Ohio.
Swofford D. L. 2000. PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates Inc. Sunderland Mass.
10.1093/nar/25.24.4876
10.1016/0021-9975(70)90053-8

Dates

Type	When
Created	20 years, 9 months ago (Nov. 4, 2004, 8:09 p.m.)
Deposited	3 years, 5 months ago (March 4, 2022, 9:42 p.m.)
Indexed	1 month, 2 weeks ago (July 9, 2025, 7:01 p.m.)
Issued	20 years, 9 months ago (Nov. 1, 2004)
Published	20 years, 9 months ago (Nov. 1, 2004)
Published Print	20 years, 9 months ago (Nov. 1, 2004)

Funders 0

None

BibTeX

@article{Draghi_2004, title={Characterization of “ Candidatus Piscichlamydia salmonis” (Order Chlamydiales ), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon ( Salmo salar )}, volume={42}, ISSN={1098-660X}, url={http://dx.doi.org/10.1128/jcm.42.11.5286-5297.2004}, DOI={10.1128/jcm.42.11.5286-5297.2004}, number={11}, journal={Journal of Clinical Microbiology}, publisher={American Society for Microbiology}, author={Draghi, Andrew and Popov, Vsevolod L. and Kahl, Melissa M. and Stanton, James B. and Brown, Corrie C. and Tsongalis, Gregory J. and West, A. Brian and Frasca, Salvatore}, year={2004}, month=nov, pages={5286–5297} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        9
      ]
    ],
    "date-time": "2025-07-09T23:01:50Z",
    "timestamp": 1752102110605
  },
  "reference-count": 32,
  "publisher": "American Society for Microbiology",
  "issue": "11",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2004,
            11,
            1
          ]
        ],
        "date-time": "2004-11-01T00:00:00Z",
        "timestamp": 1099267200000
      },
      "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": [
      [
        2004,
        11
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            To characterize intracellular gram-negative bacteria associated with epitheliocystis in farmed Atlantic salmon (\n            <jats:italic>Salmo salar</jats:italic>\n            ), gills with proliferative lesions were collected for histopathology, conventional transmission and immunoelectron microscopy, in situ hybridization, and DNA extraction during epitheliocystis outbreaks in Ireland and Norway in 1999 and 2000, respectively, and compared by ultrastructure and immunoreactivity to nonproliferative gills from Ireland archived in 1995. Genomic DNA from proliferative gills was used to amplify 16S ribosomal DNA (rDNA) for molecular phylogenetic analyses. Epitheliocystis inclusions from proliferative gills possessed variably elongate reticulate bodies, examples of binary fission, and vacuolated and nonvacuolated intermediate bodies, whereas inclusions in nonproliferative gills had typical chlamydial developmental stages plus distinctive head-and-tail cells. Immunogold processing using anti-chlamydial lipopolysaccharide antibody labeled reticulate bodies from proliferative and nonproliferative gills. 16S rDNA amplified directly from Irish (1999) and Norwegian (2000) gill samples demonstrated 99% nucleotide identity, and riboprobes transcribed from cloned near-full-length 16S rDNA amplicons from Norwegian gills hybridized with inclusions in proliferative lesions from Irish (1999) and Norwegian (2000) sections. A 1,487-bp consensus 16S rRNA gene sequence representing the chlamydia-like bacterium (CLB) from proliferative gills had the highest percent nucleotide identity with endosymbionts of\n            <jats:italic>Acanthamoeba</jats:italic>\n            spp. (order\n            <jats:italic>Chlamydiales</jats:italic>\n            ). Molecular phylogenetic relationships inferred from 16S rRNA gene sequences using distance and parsimony indicated that the CLB from proliferative gills branched with members of the order\n            <jats:italic>Chlamydiales</jats:italic>\n            . \u201c\n            <jats:italic>Candidatus</jats:italic>\n            Piscichlamydia salmonis\u201d is proposed for the CLB associated with epitheliocystis from proliferative gills of Atlantic salmon, which exhibits developmental stages different from those identified in nonproliferative gills.\n          </jats:p>",
  "DOI": "10.1128/jcm.42.11.5286-5297.2004",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        11,
        5
      ]
    ],
    "date-time": "2004-11-05T01:09:22Z",
    "timestamp": 1099616962000
  },
  "page": "5286-5297",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 119,
  "title": "Characterization of \u201c\n            <i>Candidatus</i>\n            Piscichlamydia salmonis\u201d (Order\n            <i>Chlamydiales</i>\n            ), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon (\n            <i>Salmo salar</i>\n            )",
  "prefix": "10.1128",
  "volume": "42",
  "author": [
    {
      "suffix": "II",
      "given": "Andrew",
      "family": "Draghi",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Pathobiology and Veterinary Science, University of Connecticut, Storrs, Connecticut"
        }
      ]
    },
    {
      "given": "Vsevolod L.",
      "family": "Popov",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Electron Microscopy Laboratory, Department of Pathology, The University of Texas Medical Branch, Galveston, Texas"
        }
      ]
    },
    {
      "given": "Melissa M.",
      "family": "Kahl",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathobiology and Veterinary Science, University of Connecticut, Storrs, Connecticut"
        }
      ]
    },
    {
      "given": "James B.",
      "family": "Stanton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia"
        }
      ]
    },
    {
      "given": "Corrie C.",
      "family": "Brown",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia"
        }
      ]
    },
    {
      "given": "Gregory J.",
      "family": "Tsongalis",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathology, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire"
        }
      ]
    },
    {
      "given": "A. Brian",
      "family": "West",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathology, New York University Medical Center, New York, New York"
        }
      ]
    },
    {
      "suffix": "Jr.",
      "given": "Salvatore",
      "family": "Frasca",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pathobiology and Veterinary Science, University of Connecticut, Storrs, Connecticut"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/aem.63.1.115-121.1997"
    },
    {
      "key": "e_1_3_2_3_2",
      "first-page": "159",
      "volume": "28",
      "year": "1984",
      "unstructured": "Avakyan, A. A., and V. L. Popov. 1984. Rickettsiae and chlamydiae: comparative electron microscopic studies. Acta Virol.28:159-173.",
      "journal-title": "Acta Virol."
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/dao004009"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/030098589803500301"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/dao037061"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-51-6-2145"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.169.12.5678-5685.1987"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-47-2-461"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-49-2-415"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1558-5646.1985.tb00420.x"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.66.6.2613-2619.2000"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.64.10.3599-3606.1998"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1179/his.1994.17.4.313"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/104063879600800206"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/417338"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02219125"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00221287-146-5-1231"
    },
    {
      "key": "e_1_3_2_19_2",
      "first-page": "213",
      "year": "1981",
      "unstructured": "Ito, S., and Y. Rikihisa. 1981. Techniques for electron microscopy of rickettsiae, p. 213-227. In W. Burgdorfer and R. L. Anacker (ed.), Rickettsiae and rickettsial diseases. Academic Press, New York, N.Y.",
      "journal-title": "Rickettsiae and rickettsial diseases"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-49-2-815"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1995.mmi_18030391.x"
    },
    {
      "key": "e_1_3_2_22_2",
      "first-page": "405",
      "volume": "100",
      "year": "1976",
      "unstructured": "McDowell, E. M., and B. F. Trump. 1976. Histologic fixatives suitable for diagnostic light and electron microscopy. Arch. Pathol. Lab. Med.100:405-406.",
      "journal-title": "Arch. Pathol. Lab. Med."
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1577/1548-8667(1998)010<0043:AMSOTE>2.0.CO;2"
    },
    {
      "key": "e_1_3_2_24_2",
      "first-page": "205",
      "year": "1996",
      "unstructured": "Palumbi, S. R. 1996. Nucleic acids II: the polymerase chain reaction, p. 205-248. In D. M. Hillis, C. Moritz, and B. K. Mable (ed.), Molecular systematics, 2nd ed. Sinauer Associates, Inc., Sunderland, Mass.",
      "journal-title": "Molecular systematics"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-47-4-1145"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0044-8486(77)90018-7"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.13.4195-4205.1997"
    },
    {
      "key": "e_1_3_2_28_2",
      "first-page": "489",
      "year": "1993",
      "unstructured": "Relman, D. A. 1993. Universal bacterial 16S rDNA amplification and sequencing, p. 489-495. In D. H. Pershing, T. F. Smith, F. C. Tenover, and T. J. White (ed.), Diagnostic molecular microbiology: principles and applications. American Society for Microbiology, Washington, D.C.",
      "journal-title": "Diagnostic molecular microbiology: principles and applications"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2761.1984.tb00935.x"
    },
    {
      "key": "e_1_3_2_30_2",
      "unstructured": "Sheehan D. Z. and B. B. Hrapchak. 1980. Theory and practice of histotechnology. Bettelle Press Columbus Ohio."
    },
    {
      "key": "e_1_3_2_31_2",
      "unstructured": "Swofford D. L. 2000. PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates Inc. Sunderland Mass."
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/25.24.4876"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0021-9975(70)90053-8"
    }
  ],
  "container-title": "Journal of Clinical Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JCM.42.11.5286-5297.2004",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JCM.42.11.5286-5297.2004",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        3,
        5
      ]
    ],
    "date-time": "2022-03-05T02:42:42Z",
    "timestamp": 1646448162000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JCM.42.11.5286-5297.2004"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        11
      ]
    ]
  },
  "references-count": 32,
  "journal-issue": {
    "issue": "11",
    "published-print": {
      "date-parts": [
        [
          2004,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JCM.42.11.5286-5297.2004"
  ],
  "URL": "http://dx.doi.org/10.1128/JCM.42.11.5286-5297.2004",
  "relation": {},
  "ISSN": [
    "0095-1137",
    "1098-660X"
  ],
  "subject": [],
  "container-title-short": "J Clin Microbiol",
  "published": {
    "date-parts": [
      [
        2004,
        11
      ]
    ]
  },
  "assertion": [
    {
      "value": "2004-03-16",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2004-07-05",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2004-11-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}