{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T04:37:11Z","timestamp":1788928631707,"version":"build-2803163510"},"reference-count":56,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,3,9]],"date-time":"2022-03-09T00:00:00Z","timestamp":1646784000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>\n                    The present study describes a simultaneous infection of a novel\n                    <jats:italic>Chlamydia<\/jats:italic>\n                    -like organism (CLO) with a Myxozoa parasite,\n                    <jats:italic>Henneguya<\/jats:italic>\n                    sp. in snakeskin gourami\n                    <jats:italic>Trichopodus pectoralis<\/jats:italic>\n                    in Thailand. A new CLO is proposed \u201c\n                    <jats:italic>Candidatus<\/jats:italic>\n                    Piscichlamydia trichopodus\u201d (CPT) based on 16S rRNA phylogenetic analysis. Systemic intracellular CPT infection was confirmed by histological examination,\n                    <jats:italic>in situ<\/jats:italic>\n                    hybridization, PCR assay, and sequencing of 16S rRNA. This novel pathogen belongs to the order\n                    <jats:italic>Chlamydiales<\/jats:italic>\n                    but differs in certain aspects from other species. The histopathological changes associated with CPT infection were different from the typical pathological lesions of epitheliocystis caused by previously known CLO. Unlike other CLO, CPT localized in the connective tissue rather than in the epithelial cells and formed smaller clumps of intracellular bacteria that stained dark blue with hematoxylin. On the other hand, typical myxospores of the genus\n                    <jats:italic>Henneguya<\/jats:italic>\n                    with tails were observed in the gill sections. Infection with\n                    <jats:italic>Henneguya<\/jats:italic>\n                    sp. resulted in extensive destruction of the gill filaments, most likely leading to respiratory distress. Due to the frequency of co-infections and the unavailability of culture methods for CLO and\n                    <jats:italic>Henneguya<\/jats:italic>\n                    sp., it was difficult to determine which pathogens were directly responsible for the associated mortality. However, co-infections may increase the negative impact on the host and the severity of the disease. Given the commercial importance of the snakeskin gourami and its significant aquaculture potential, the findings of this study are important for further studies on disease prevention.\n                  <\/jats:p>","DOI":"10.3389\/fvets.2022.847977","type":"journal-article","created":{"date-parts":[[2022,3,10]],"date-time":"2022-03-10T13:12:09Z","timestamp":1646917929000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Co-infection of Candidatus Piscichlamydia Trichopodus (Order Chlamydiales) and Henneguya sp. (Myxosporea, Myxobolidae) in Snakeskin Gourami Trichopodus pectoralis (Regan 1910)"],"prefix":"10.3389","volume":"9","author":[{"given":"Nguyen","family":"Dinh-Hung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ha Thanh","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chayanit","family":"Soontara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Channarong","family":"Rodkhum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sukkrit","family":"Nimitkul","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prapansak","family":"Srisapoome","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pattanapon","family":"Kayansamruaj","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satid","family":"Chatchaiphan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,3,9]]},"reference":[{"key":"B1","first-page":"49","article-title":"The nomenclature of Trichopodus pectoralis Regan, 1910; Trichopus cantoris Sauvage, 1884 and Osphronemus saigonensis Borodin, 1930 (Teleostei: Peciformes: Osphronemidae)","volume":"59","author":"Paepke","year":"2009","journal-title":"Vertebr Zool"},{"key":"B2","volume-title":"Fishery and Aquaculture Statistics. Global Aquaculture Production 1950-2019 (FishstatJ)","year":""},{"key":"B3","article-title":"Statistics of Freshwater Aquaculture Production","year":"2018","journal-title":"Fisheries Development Policy and Strategy Division No. 8\/2018"},{"key":"B4","doi-asserted-by":"publisher","first-page":"210","DOI":"10.33495\/jacr_v8i10.20.168","article-title":"Occurrence of parasitic and bacterial diseases in Thai freshwater fish","volume":"8","author":"Kanchan","year":"2020","journal-title":"J Agric Crop Resh."},{"key":"B5","unstructured":"Snakeskin Gourami (Trichopodus pectoralis) Ecological Risk Screening Summary.2019"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.14411\/fp.2006.001","article-title":"Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species","volume":"53","author":"Lom","year":"2006","journal-title":"Folia Parasitol"},{"key":"B7","doi-asserted-by":"publisher","first-page":"197","DOI":"10.3354\/dao048197","article-title":"Site preference of fish myxosporeans in the gill","volume":"48","author":"Moln\u00e1r","year":"2002","journal-title":"Dis Aquat Organ."},{"key":"B8","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1007\/s11230-012-9374-7","article-title":"A checklist of new species of Henneguya Th\u00e9lohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012","volume":"83","author":"Eiras","year":"2012","journal-title":"Syst Parasitol"},{"key":"B9","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1111\/j.1365-2761.1989.tb00287.x","article-title":"guideline for the preparation of species descriptions in Myxosporea","volume":"12","author":"Lom","year":"1989","journal-title":"J Fish Dis."},{"key":"B10","first-page":"85","article-title":"Classification and Phylogenetics of Myxozoa. In: Myxozoan Evolution, Ecology and Development, eds. Okamura B, Gruhl A, Bartholomew JL","author":"Fiala","year":"2015","journal-title":"Springer International Publishing"},{"key":"B11","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1111\/j.1550-7408.2001.tb00173.x","article-title":"Recent advances in our knowledge of the Myxozoa","volume":"48","author":"Kent","year":"2001","journal-title":"J Eukaryot Microbiol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1111\/j.1095-8649.1978.tb04165.x","article-title":"Histopathological changes in fish gills infected with myxosporidian parasites of the genus Henneguya","volume":"12","author":"Dykova","year":"1978","journal-title":"J Fish Biol"},{"key":"B13","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1577\/A03-059.1","article-title":"Assay to detect the actinospore and myxospore stages of proliferative gill disease in oligochaetes and pond water","volume":"67","author":"Whitaker","year":"2005","journal-title":"N Am J Aquac."},{"key":"B14","doi-asserted-by":"publisher","first-page":"15","DOI":"10.3354\/dao020015","article-title":"Pathogenicity and seasonal occurrence of Henneguya-creplini (Protozoa, Myxosporea) on the gills of perch Perca-Fluviatilis in central Finland","volume":"20","author":"Haaparanta","year":"1994","journal-title":"Dis Aquat Organ."},{"key":"B15","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1111\/j.1365-2761.2006.00747.x","article-title":"Epitheliocystis in fish","volume":"29","author":"Nowak","year":"2006","journal-title":"J Fish Dis."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1436","DOI":"10.1111\/tbed.12908","article-title":"Epitheliocystis in fish: an emerging aquaculture disease with a global impact","volume":"65","author":"Blandford","year":"2018","journal-title":"Transbound Emerg Dis."},{"key":"B17","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1007\/s13353-015-0303-8","article-title":"Characteristics of Chlamydia-like organisms pathogenic to fish","volume":"57","author":"Pawlikowska-Warych","year":"2016","journal-title":"J Appl Genet."},{"key":"B18","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1177\/0300985817751218","article-title":"A review on chlamydial diseases in animals: still a challenge for pathologists?","volume":"55","author":"Borel","year":"2018","journal-title":"Vet Pathol."},{"key":"B19","first-page":"18","article-title":"Trends in the farming of the snakeskin gourami (Trichogaster pectoralis) in Thailand","volume":"20","author":"Yoonpundh","year":"1997","journal-title":"Naga, The WorldFish Center."},{"key":"B20","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/978-3-319-14753-6_4","article-title":"Adaptive radiation and evolution within the myxozoa. In: Myxozoan Evolution, Ecology and Development, editors. Okamura B, Gruhl A, Bartholomew JL","author":"Fiala","year":"2015","journal-title":"Springer International Publishing"},{"key":"B21","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1099\/00207713-49-2-415","article-title":"Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov and Simkaniaceae fam nov, each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms","volume":"49","author":"Everett","year":"1999","journal-title":"Int J Syst Bacteriol."},{"key":"B22","first-page":"489","year":"1993","journal-title":"Diagnostic Molecular Biology, Principles and Applications"},{"key":"B23","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1016\/j.aquaculture.2019.03.007","article-title":"Epitheliocystis in rohu Labeo rohita (Hamilton, 1822) is caused by novel Chlamydiales","volume":"505","author":"Sood","year":"2019","journal-title":"Aquaculture"},{"key":"B24","doi-asserted-by":"publisher","first-page":"5286","DOI":"10.1128\/JCM.42.11.5286-5297.2004","article-title":"Characterization of \u201cCandidatus piscichlamydia salmonis\u201d (order Chlamydiales), a chlamydia-like bacterium associated with epitheliocystis in farmed Atlantic salmon (Salmo salar)","volume":"42","author":"Draghi","year":"2004","journal-title":"J Clin Microbiol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol Biol Evol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1111\/jfd.13367","article-title":"Dissecting the localization of Tilapia tilapinevirus in the brain of the experimentally infected Nile tilapia, Oreochromis niloticus (L)","volume":"44","author":"Dinh-Hung","year":"2021","journal-title":"J Fish Dis."},{"key":"B27","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1080\/713610404","article-title":"Increasing diversity within Chlamydiae","volume":"29","author":"Corsaro","year":"2003","journal-title":"Crit Rev Microbiol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1146\/annurev.micro.62.081307.162818","volume":"62","author":"Horn","year":"2008","journal-title":"Annu Rev Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.vetmic.2014.01.022","article-title":"Chlamydial infections of fish: diverse pathogens and emerging causes of disease in aquaculture species","volume":"170","author":"Stride","year":"2014","journal-title":"Vet Microbiol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1556\/004.2017.003","article-title":"Diverse Chlamydia-like agents associated with epitheliocystis infection in two cyprinid fish species, the common carp (Cyprinus carpio L","volume":"65","author":"Sellyei","year":"2017","journal-title":"Acta Vet Hung."},{"key":"B31","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1292\/jvms.67.119","article-title":"Epitheliocystis in carp (Cyprinus carpio) in South Korea","volume":"67","author":"Kim","year":"2005","journal-title":"J Vet Med Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"e66840","DOI":"10.1371\/journal.pone.0066840","article-title":"\u2018Cand. Actinochlamydia clariaeh gen nov, sp nov, a unique intracellular bacterium causing epitheliocystis in catfish (Clarias gariepinus) in Uganda","volume":"8","author":"Steigen","year":"2013","journal-title":"PLoS ONE."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1590","DOI":"10.1128\/AEM.02899-12","article-title":"Molecular characterization of \u201cCandidatus Parilichlamydia carangidicola,\u201d a novel Chlamydia-like epitheliocystis agent in yellowtail kingfish, Seriola lalandi (Valenciennes), and the proposal of a new family, \u201cCandidatus Parilichlamydiaceae\u201d fam. nov (order Chlamydiales)","volume":"79","author":"Stride","year":"2013","journal-title":"Appl Environ Microbiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"4914","DOI":"10.1128\/AEM.00746-13","article-title":"Molecular characterization of \u201cCandidatus Similichlamydia latridicola\u201d gen. nov, sp nov (Chlamydiales: \u201cChlamydial Parilichlamydiaceaeary a novel Chlamydia-like epitheliocystis agent in the striped trumpeter, Latris lineata (Forster)","volume":"79","author":"Stride","year":"2013","journal-title":"Appl Environ Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"e82889","DOI":"10.1371\/journal.pone.0082889","article-title":"\u201cCandidatus Similichlamydia laticola\u201d, a novel Chlamydia-like agent of epitheliocystis in seven consecutive cohorts of farmed Australian barramundi, Lates calcarifer (Bloch)","volume":"8","author":"Stride","year":"2013","journal-title":"PLoS ONE."},{"key":"B36","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1111\/jfd.12711","article-title":"Candidatus Actinochlamydia pangasiae sp nov (Chlamydiales, Actinochlamydiaceae), a bacterium associated with epitheliocystis in Pangasianodon hypophthalmus","volume":"41","author":"Sood","year":"2018","journal-title":"J Fish Dis."},{"key":"B37","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1016\/0022-2011(85)90010-2","article-title":"A systemic microbial disease in the Dungeness crab, Cancer magister, caused by a Chlamydia-like organism","volume":"45","author":"Sparks","year":"1985","journal-title":"J Invertebr Pathol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1111\/j.1365-2761.1984.tb00916.x","article-title":"The developmental cycle of epitheliocystis in carp, Cyprinus carpio L","volume":"7","author":"Paperna","year":"1984","journal-title":"J Fish Dis."},{"key":"B39","doi-asserted-by":"publisher","first-page":"199","DOI":"10.2331\/suisan.52.199","article-title":"A light and electron microscopic study on epitheliocystis disease in cultured fishes","volume":"52","author":"Miyazaki","year":"1986","journal-title":"Nippon Suisan Gakkaishi."},{"key":"B40","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1111\/j.1365-2761.1988.tb00744.x","article-title":"Ultrastructural observations on the causative agent of epitheliocystis in the brown bullhead, Ictalurus nebulosus Lesueur, from Ontario and a comparison with the Chlamydiae of higher vertebrates","volume":"11","author":"Desser","year":"1988","journal-title":"J Fish Dis."},{"key":"B41","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1577\/1548-8667(1998)010&lt;0043:AMSOTE&gt;2.0.CO;2","article-title":"A morphological study of the epitheliocystis agent in farmed Atlantic Salmon","volume":"10","author":"Nylund","year":"1998","journal-title":"J Aquat Anim Health"},{"key":"B42","doi-asserted-by":"publisher","first-page":"59","DOI":"10.3354\/dao057059","article-title":"Protozoal and epitheliocystis-like infections in the introduced bluestripe snapper Lutjanus kasmira in Hawaii","volume":"57","author":"Work","year":"2003","journal-title":"Dis Aquat Organ."},{"key":"B43","doi-asserted-by":"publisher","first-page":"61","DOI":"10.3354\/dao037061","article-title":"Epitheliocystis agents in sea bream Sparus aurata: morphological evidence for two distinct Chlamydia-like developmental cycles","volume":"37","author":"Crespo","year":"1999","journal-title":"Dis Aquat Organ."},{"key":"B44","doi-asserted-by":"publisher","first-page":"131","DOI":"10.3389\/fphys.2016.00131","article-title":"Epitheliocystis distribution and dharacterization in brown trout (Salmo trutta) from the headwaters of two major European rivers, the Rhine and Rhone","volume":"7","author":"Guevara Soto","year":"2016","journal-title":"Front Physiol."},{"key":"B45","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/978-3-319-14753-6_6","article-title":"Approaches for characterizing myxozoan species. In: Okamura B, Gruhl A, Bartholomew JL, editors","author":"Atkinson","year":"2015","journal-title":"Myxozoan Evolution, Ecology and Development"},{"key":"B46","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1016\/j.ijpara.2019.02.009","article-title":"Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade","volume":"48","author":"Liu","year":"2019","journal-title":"Int J Parasitol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1023\/A:1015016312195","article-title":"Synopsis of the species of the genus Henneguya Th\u00e9lohan, 1892 (Myxozoa: myxosporea: myxobolidae","volume":"52","author":"Eiras","year":"2002","journal-title":"Syst Parasitol."},{"key":"B48","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1007\/978-3-319-14753-6_16","article-title":"Specificity of infection sites in vertebrate hosts","author":"Moln\u00e1r","year":"2015","journal-title":"Myxozoan Evolution, Ecology and Development"},{"key":"B49","first-page":"897","article-title":"Prevalence of Henneguya branchialis in Catfish (Clarias gariepinus) in Ismailia, Egypt","volume":"12","author":"Sabri","year":"2010","journal-title":"Int J Agric Biol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.aqrep.2015.11.004","article-title":"An outbreak of myxozoan parasites in farmed freshwater fish Colossoma macropomum (Cuvier, 1818) (Characidae, Serrasalminae) in the Amazon region, Brazil","volume":"3","author":"Videira","year":"2016","journal-title":"Aquac."},{"key":"B51","doi-asserted-by":"publisher","first-page":"686","DOI":"10.1645\/19-28","article-title":"Pathologic changes associated with respiratory compromise and morbidity due to massive interlamellar Henneguya exilis infection in Channel \u00d7 Blue Hybrid Catfish","volume":"105","author":"Stilwell","year":"2019","journal-title":"J Parasitol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"207","DOI":"10.3354\/dao02968","article-title":"Morphology, histology and phylogeny of Henneguya sinova sp. nov (Myxobolidae: Myxozoa) infecting gills of Parablennius tentacularis in the Black Sea, Turkey","volume":"118","author":"\u00d6zer","year":"2016","journal-title":"Dis Aquat Organ."},{"key":"B53","doi-asserted-by":"publisher","first-page":"3327","DOI":"10.1007\/s00436-019-06533-1","article-title":"new myxozoan species Henneguya unitaeniata sp. nov (Cnidaria: Myxosporea) on gills of Hoplerythrinus unitaeniatus from Mato Grosso State, Brazil","volume":"118","author":"\u00dangari","year":"2019","journal-title":"Parasitol Res."},{"key":"B54","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1111\/j.1365-2761.2005.00655.x","article-title":"Henneguya pagri n. sp (Myxozoa: Myxosporea) causing cardiac henneguyosis in red sea bream, Pagrus major (Temminck & Schlegel)","volume":"28","author":"Yokoyama","year":"2005","journal-title":"J Fish Dis."},{"key":"B55","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1007\/s12639-019-01183-7","article-title":"Henneguyosis in gills of Metynnis hypsauchen: an Amazon freshwater fish","volume":"44","author":"Figueredo","year":"2020","journal-title":"J Parasit Dis."},{"key":"B56","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1111\/j.1365-2761.2005.00662.x","article-title":"Successful treatment of largemouth bass, Micropterus salmoides (L), with epitheliocystis hyperinfection","volume":"28","author":"Goodwin","year":"2005","journal-title":"J Fish Dis."}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.847977\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,10]],"date-time":"2022-03-10T13:12:24Z","timestamp":1646917944000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.847977\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,9]]},"references-count":56,"alternative-id":["10.3389\/fvets.2022.847977"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2022.847977","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.06.01.446678","asserted-by":"object"}]},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,9]]},"article-number":"847977"}}