Citation: | YANG Yi-Jing, YIN Qi, ZHAO Xiao-Jing, WEI Qiang, LIU Xin-Hua. SKIN MICROBIOTA ANALYSIS OF GIBEL CARP (CARASSIUS AURATUS GIBELIO) INFECTED BY THELOHANELLUS WUHANENSIS XIAO & CHEN, 1993[J]. ACTA HYDROBIOLOGICA SINICA. DOI: 10.7541/2025.2024.0403 |
Thelohanellus wuhanensis Xiao & Chen, 1993, a pathogen of “skin myxosporidiosis”, infects the skin of gibel carp (Carassius auratus gibelio), and can cause significant mortality in juvenile fish. Currently, researches on T. wuhanensis has primarily focused on its identification, pathogenicity, and life cycle, with little attention has been paid to the potential bacterial secondary infections it may cause. Here, the skin microbiota analysis (including the species diversity, composition, and abundance) of Carassius auratus gibelio infected by T. wuhanensis was conducted using high-throughput 16S rDNA sequencing. The results indicated that both the healthy and infected groups of C. auratus gibelio possessed a total of 939 Operational Taxonomic Units (OTUs) were obtained, belonging to 30 phyla, 80 classes, 188 orders, 295 families, 475 genera, and 692 species. The healthy group had 308 unique OTUs, while the infected group had 342 unique OTUs. The α-diversity analysis revealed significantly higher microbial diversity but significantly lower richness in the infected group compared with the healthy group. In addition, the β-diversity analysis demonstrated significant differences in the structure of skin microbial communities between the healthy and infected groups. At the phylum level, Firmicutes, Proteobacteria, Cyanobacteria, Actinobacteria, and Bacteroidetes were the dominant taxa in both the healthy and infected groups, although differences in abundance were observed. At the genus level, 20 genera exhibited a relative abundance exceeding 1%. The dominant genus in the healthy group was Lactococcus, while Achromobacter was the most prevalent in the infected group, representing 58.99% and 48.67% of the total microbial abundance, respectively. The results of the linear discriminant analysis (LDA) and functional prediction indicated a significant increase in both the abundance of pathogenic bacteria and the potential pathogenicity of the microbiota in the infected group in comparison to the healthy group. In conclusion, the infection of T. wuhanensis can disrupt the skin microbiota of C. auratus gibelio, leading to the possibility of secondary bacterial infection.
[1] |
Guivier E, Pech N, Chappaz R, et al. Microbiota associated with the skin, gills, and gut of the fish Parachondrostoma toxostoma from the Rhône basin [J]. Freshwater Biology, 2020, 65(3): 446-459. doi: 10.1111/fwb.13437
|
[2] |
张艳敏, 杨国坤, 李克克, 等. 鱼类黏膜层微生物研究进展 [J]. 水产学报, 2022, 46(6): 1117-1127.]
Zhang Y M, Yang G K, Li K K, et al. Research progress of mucosal microorganisms of fish [J]. Journal of Fisheries of China, 2022, 46(6): 1117-1127. [
|
[3] |
田甜, 张建明, 张德志, 等. 健康和患病中华鲟皮肤黏膜层微生物菌群结构特征 [J]. 中国水产科学, 2023, 30(10): 1259-1270.]
Tian T, Zhang J M, Zhang D Z, et al. Analysis on skin mucosa microbial community structure of healthy and diseased Chinese sturgeon (Acipenser sinensis) [J]. Journal of Fishery Sciences of China, 2023, 30(10): 1259-1270. [
|
[4] |
王雪芹, 阳涛. 我国鱼类寄生虫病的防治策略及研究现状 [J]. 水产养殖, 2020, 41(11): 5-10.] doi: 10.3969/j.issn.1004-2091.2020.11.002
Wang X Q, Yang T. Prevention and control strategies and research status of fish parasitosis in China [J]. Journal of Aquaculture, 2020, 41(11): 5-10. [ doi: 10.3969/j.issn.1004-2091.2020.11.002
|
[5] |
Wang Z, Zhou T, Yang H, et al. First diagnosis of ectoparasitic ciliates (Trichodina and Chilodonella) on farmed juvenile yellow catfish, Tachysurus fulvidraco in China [J]. Aquaculture Research, 2019, 50(11): 3275-3285. doi: 10.1111/are.14285
|
[6] |
Abdelkhalek N K, El-Adl M A, Salama M F, et al. Molecular identification of Trichodina compacta van As and basson, 1989 (Ciliophora: Peritrichia) from cultured Oreochromis niloticus in Egypt and its impact on immune responses and tissue pathology [J]. Parasitology Research, 2018, 117(6): 1907-1914. doi: 10.1007/s00436-018-5883-x
|
[7] |
贺扬, 樊威, 陈杰, 等. 瓦氏黄颡鱼多子小瓜虫病的组织病理学观察 [J]. 云南农业大学学报(自然科学), 2020, 35(6): 1016-1022.]
He Y, Fan W, Chen J, et al. Histopathological Observation of Pelteobagrus vachelli infected with Ichthyophthirius multifiliis [J]. Journal of Yunnan Agricultural University (Natural Science), 2020, 35(6): 1016-1022. [
|
[8] |
Huang K, Li X, Yue X, et al. Outbreak of Cryptocaryon irritans infection in silver pomfret Pampus argenteus cultured in China [J]. Diseases of Aquatic Organisms, 2022(154): 59-68. doi: 10.3354/dao03728
|
[9] |
Zeng S, Duan Y, Li X, et al. Effects of Cryptocaryon irritans infection on the histopathology, oxidative stress, immune response, and intestinal microbiota in the orange-spotted grouper Epinephelus coioides [J]. Fish & Shellfish Immunology, 2023(133): 108562.
|
[10] |
Ramadan R M, Mahdy O A, El-Saied M A, et al. Novel insights into immune stress markers associated with myxosporeans gill infection in nile tilapia (molecular and immunohistochemical studies) [J]. PLoS One, 2024, 19(6): e0303702. doi: 10.1371/journal.pone.0303702
|
[11] |
Ibrahim M M, Baghdadi H B, Shahin K, et al. Dasyrhynchus giganteus plerocercoids encysting in the musculature of Indian halibut (Psettodes erumei): seasonal prevalence, Morpho-molecular characterization, and histopathological alterations [J]. BMC Veterinary Research, 2024, 20(1): 332. doi: 10.1186/s12917-024-04156-y
|
[12] |
Buchmann K. Control of parasitic diseases in aquaculture [J]. Parasitology, 2022, 149(14): 1985-1997. doi: 10.1017/S0031182022001093
|
[13] |
Liu Y, Yuan J, Jia L, et al. Supplemental description of Thelohanellus wuhanensis Xiao & Chen, 1993 (Myxozoa: Myxosporea) infecting the skin of Carassius auratus gibelio (Bloch): Ultrastructural and histological data [J]. Parasitology International, 2014, 63(3): 489-491. doi: 10.1016/j.parint.2014.01.003
|
[14] |
陆宏达, 任芳芳, 贾相相, 等. 异育银鲫武汉单极虫病发生、发展、消退和消失的病理变化与PCR分析 [J]. 水产学报, 2018, 42(11): 1817-1828.]
Lu H D, Ren F F, Jia X X, et al. Pathology and PCR assay of Thelohanellus wuhanensis disease in Allogynogenetic crucian carp (Carassius auratus gibelio) in the periods of occurrence, development, fade and disappearance [J]. Journal of Fisheries of China, 2018, 42(11): 1817-1828. [
|
[15] |
Lom J, Arthur J R. A guideline for the preparation of species descriptions in Myxosporea [J]. Journal of Fish Diseases, 1989, 12(2): 151-156. doi: 10.1111/j.1365-2761.1989.tb00287.x
|
[16] |
Hall T. Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/nt [J]. Nucleic Acids Symposium Series, 1999, 41(41): 95-98.
|
[17] |
Thompson J D, Gibson T J, Plewniak F, et al. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools [J]. Nucleic Acids Research, 1997, 25(24): 4876-4882. doi: 10.1093/nar/25.24.4876
|
[18] |
Posada D. jModelTest: phylogenetic model averaging [J]. Molecular Biology and Evolution, 2008, 25(7): 1253-1256. doi: 10.1093/molbev/msn083
|
[19] |
Schloss P D, Westcott S L, Ryabin T, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities [J]. Applied and Environmental Microbiology, 2009, 75(23): 7537-7541. doi: 10.1128/AEM.01541-09
|
[20] |
Caporaso J G, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data [J]. Nature Methods, 2010, 7(5): 335-336. doi: 10.1038/nmeth.f.303
|
[21] |
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation [J]. Genome Biology, 2011, 12(6): R60. doi: 10.1186/gb-2011-12-6-r60
|
[22] |
Ward T L, Larson J, Meulemans J, et al. BugBase predicts organism-level microbiome phenotypes [J]. BioRxiv, 2017: 133462.
|
[23] |
Ross A A, Rodrigues Hoffmann A, Neufeld J D. The skin microbiome of vertebrates [J]. Microbiome, 2019, 7(1): 79. doi: 10.1186/s40168-019-0694-6
|
[24] |
Byrd A L, Belkaid Y, Segre J A. The human skin microbiome [J]. Nature Reviews Microbiology, 2018, 16(3): 143-155. doi: 10.1038/nrmicro.2017.157
|
[25] |
Minniti G, Hagen L H, Porcellato D, et al. The skin-mucus microbial community of farmed atlantic salmon (Salmo salar) [J]. Frontiers in Microbiology, 2017(8): 2043. doi: 10.3389/fmicb.2017.02043
|
[26] |
Svendsen Y S, Bøgwald J. Influence of artificial wound and non-intact mucus layer on mortality of Atlantic salmon (Salmo salar L.) following a bath challenge with Vibrio anguillarum and Aeromonas salmonicida [J]. Fish & Shellfish Immunology, 1997, 7 (5): 317-325.
|
[27] |
Sultana S, Khan M N, Hossain M S, et al. Community structure and functional annotations of the skin microbiome in healthy and diseased catfish, Heteropneustes fossilis [J]. Frontiers in Microbiology, 2022(13): 856014. doi: 10.3389/fmicb.2022.856014
|
[28] |
Parshukov A N, Kashinskaya E N, Simonov E P, et al. Variations of the intestinal gut microbiota of farmed rainbow trout, Oncorhynchus mykiss (Walbaum), depending on the infection status of the fish [J]. Journal of Applied Microbiology, 2019, 127(2): 379-395. doi: 10.1111/jam.14302
|
[29] |
Colin Y, Molbert N, Berthe T, et al. Dysbiosis of fish gut microbiota is associated with helminths parasitism rather than exposure to PAHs at environmentally relevant concentrations [J]. Scientific Reports, 2022, 12(1): 11084. doi: 10.1038/s41598-022-15010-2
|
[30] |
Huang Z, Zhan M, Cheng G, et al. IHNV infection induces strong mucosal immunity and changes of microbiota in trout intestine [J]. Viruses, 2022, 14(8): 1838. doi: 10.3390/v14081838
|
[31] |
Zhang X, Ding L, Yu Y, et al. The change of teleost skin commensal microbiota is associated with skin mucosal transcriptomic responses during parasitic infection by Ichthyophthirius multifillis [J]. Frontiers in Immunology, 2018(9): 2972. doi: 10.3389/fimmu.2018.02972
|
[32] |
Kashinskaya E N, Simonov E P, Andree K B, et al. Microbial community structure in a host- parasite system: the case of Prussian carp and its parasitic crustaceans [J]. Journal of Applied Microbiology, 2021, 131(4): 1722-1741. doi: 10.1111/jam.15071
|
[33] |
Mathieu-Bégné E, Blanchet S, Rey O, et al. A longitudinal survey in the wild reveals major shifts in fish host microbiota after parasite infection [J]. Molecular Ecology, 2023, 32(11): 3014-3024. doi: 10.1111/mec.16901
|
[34] |
Jordan C K I, Brown R L, Larkinson M L Y, et al. Symbiotic Firmicutes establish mutualism with the host via innate tolerance and resistance to control systemic immunity [J]. Cell Host & Microbe, 2023, 31 (9): 1433-1449.
|
[35] |
Llewellyn M S, Leadbeater S, Garcia C, et al. Parasitism perturbs the mucosal microbiome of Atlantic Salmon [J]. Scientific Reports, 2017(7): 43465. doi: 10.1038/srep43465
|
[36] |
Mondal H K, Maji U J, Mohanty S, et al. Alteration of gut microbiota composition and function of Indian major carp, rohu (Labeo rohita) infected with Argulus siamensis [J]. Microbial Pathogenesis, 2022(164): 105420. doi: 10.1016/j.micpath.2022.105420
|
[37] |
Johnson E L, Heaver S L, Walters W A, et al. Microbiome and metabolic disease: revisiting the bacterial Phylum Bacteroidetes [J]. Journal of Molecular Medicine, 2017, 95(1): 1-8.
|
[38] |
Meng K F, Ding L G, Wu S, et al. Interactions between commensal microbiota and mucosal immunity in teleost fish during viral infection with SVCV [J]. Frontiers in Immunology, 2021(12): 654758. doi: 10.3389/fimmu.2021.654758
|
[39] |
de Bruijn I, Liu Y, Wiegertjes G F, et al. Exploring fish microbial communities to mitigate emerging diseases in aquaculture [J]. FEMS Microbiology Ecology, 2018, 94(1): 4675208.
|
[40] |
Fu P P, Xiong F, Feng W W, et al. Effect of intestinal tapeworms on the gut microbiota of the common carp, Cyprinus carpio [J]. Parasites & Vectors, 2019, 12(1): 252.
|
[41] |
马白鸽, 魏喜红, 孟祥佳, 等. 伯克霍尔德氏菌在植物病害生物防治中的研究进展 [J]. 农业研究与应用, 2023, 36(3): 1-8.] doi: 10.3969/j.issn.2095-0764.2023.03.001
Ma B G, Wei X H, Meng X J, et al. Advancements in study on Burkholderia for plant disease biocontrol [J]. Agricultural Research and Application, 2023, 36(3): 1-8. [ doi: 10.3969/j.issn.2095-0764.2023.03.001
|
[42] |
陈晖, 傅锳洁, 王琦, 等. 2005—2020年我国唐菖蒲伯克霍尔德氏菌中毒事件流行病学分析 [J]. 中国食品卫生杂志, 2022, 34(6): 1336-1341.]
Chen H, Fu Y J, Wang Q, et al. Analysis of epidemiological characteristics of Burkholderia gladioli poisoning in China from 2005 to 2020 [J]. Chinese Journal of Food Hygiene, 2022, 34(6): 1336-1341. [
|
[43] |
Li X, Bao X, Qiao G, et al. First study of bacteremia caused by Herbaspirillum huttiense in China: a brief research report and literature review [J]. Frontiers in Cellular and Infection Microbiology, 2022(12): 882827. doi: 10.3389/fcimb.2022.882827
|
[44] |
Benitez B N, Poudel M, Jones J B, et al. First report of Herbaspirillum sp. causing leaf spots on Boston fern (Nephrolepis exaltata) in Florida [J]. Plant Disease, 2023, 107(10): 3277.
|
[45] |
Cao S, Geng Y, Yu Z, et al. Acinetobacter lwoffii, an emerging pathogen for fish in Schizothorax genus in China [J]. Transboundary and Emerging Diseases, 2018, 65(6): 1816-1822. doi: 10.1111/tbed.12957
|
[46] |
Mauel M J, Miller D L. Piscirickettsiosis and piscirickettsiosis-like infections in fish: a review [J]. Veterinary Microbiology, 2002, 87(4): 279-289. doi: 10.1016/S0378-1135(02)00085-8
|
[47] |
邹昊博, 薛淑群, 吕晓楠, 等. 1株鲤源致病性铜绿假单胞菌的分离鉴定及药敏试验 [J]. 中国畜牧兽医, 2023, 50(11): 4703-4713.]
Zou H B, Xue S Q, Lyu X N, et al. Isolation, identification and drug sensitivity test of a pathogenic strain of pseudomonas aeruginosa from common carp [J]. China Animal Husbandry & Veterinary Medicine, 2023, 50(11): 4703-4713. [
|