Exemplifying ‘pathobiome’ concept through case study: Co-infection with Vibrio harveyi, Photobacterium damsela and Cryptocaryon irritans in Salema (Sarpa salpa)

Year 2022, Volume: 6 Issue: 3, 110 - 115, 31.12.2022

Hijran Yavuzcan , Faik Sertel Secer , Bilgenur Harmanşa Yılmaz , Münir Ahmet Tunar

https://doi.org/10.30704/http-www-jivs-net.1128614

Cited By: 2

Abstract

A pathobiome approach has been revealed as a set of organisms (i.e. prokaryotic, eukaryotic, and virus associations) in the aquatic environment that interact with the host (fish) to cause disease. The approach of the one pathogen–one disease is not wholly satisfactory to comment on the impairment of health status and disease process in fish. To exemplify the pathobiome concept, we present a fish disease in which more than one pathogen and possible synergistic interaction of inadequate water quality. In this case, the heavy mortalities were observed in Salema (Sarpa salpa) from an exhibition aquaria. Bacterial identification with matrix-assisted laser desorption ionization/time-of-flight mass spectrometry (MALDI-TOF MS) showed the pathogen bacteria species of vibrio and photobacterium. In the parasitic examination, the invasion of marine ciliata, Cryptocaryon irritans was observed in the diseased fish. Moreover, poor water quality was considered as contributing factor to disease emergence in this case. The co-existence of pathogen Vibrio species (Vibrio harveyi) and Photobacterium damsela with its subspecies (subsp. damsela and subsp. piscicida) as well as marine ciliata, C. irritans for a description of a disease picture in a marine fish species are reported for the first time, providing an example of a pathobiome paradigm.

Keywords

Pathobiome, aquatic bacteria, ciliata

Supporting Institution

-

Project Number

-

Thanks

-

References

• Bass, D., Stentiford, G. D., Wang, H. C., Koskella, B., & Tyler, C. R. (2019). The Pathobiome in Animal and Plant Diseases. Trends in Ecology and Evolution, 34(11), 996-1008. https://doi.org/10.1016/j.tree.2019.07.012
• Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. Revisited. The Journal of Parasitology, 83(4), 575. https://doi.org/10.2307/3284227
• Cascarano, M. C., Stavrakidis-Zachou, O., Mladineo, I., Thompson K. D., Papandroulakis, N., & Katharios, P. (2021). Mediterranean aquaculture in a changing climate: Temperature effects on pathogens and diseases of three farmed fish species. Pathogens, 10(9). https://doi.org/10.3390/pathogens10091205
• Cheng, W. C., Jan, I. S., Chen, J. M., Teng, S. H., Teng, L. J., Sheng, W. H., Ko, W. C., & Hsueh, P. R. (2015). Evaluation of the bruker biotyper matrix-assisted laser desorption ionization-time of flight mass spectrometry system for identification of blood isolates of vibrio species. Journal of Clinical Microbiology, 53(5),1741-1744. https://doi.org/10.1128/JCM.00105-15
• Colorni, A. (1985). Aspects of the biology of Cryptocaryon irritans, and hyposalinity as a control measure in cultured gilt-head sea bream Sparus aurata. Diseases Aquatic Organisms, 1, 19-22. doi: 10.3354/dao001019
• Dickerson, H. W., & Dawe, D. L. (2006). Ichthyophthirius multifiliis and Cryptocaryon irritans (phylum Ciliophora). Fish diseases and disorders, Protozoan and Metazoan Infections, (2nd ed.) 1:116-153. Wallingford, UK.
• Dieckmann, R., Strauch, E., & Alter, T. (2010). Rapid identification and characterization of Vibrio species using whole-cell MALDI-TOF mass spectrometry. Journal of Applied Microbiology, 109, 199-211. https://doi.org/10.1111/j.1365-2672.2009.04647.x
• El-Son, M. A., Nofal, M. I., & Abdel-Latif, H. M. R. (2021). Co-infection of Aeromonas hydrophila and Vibrio parahaemolyticus isolated from diseased farmed striped mullet (Mugil cephalus) in Manzala, Egypt – A case report. Aquaculture, 530(July 2020), 735738. https://doi.org/10.1016/j.aquaculture.2020.735738
• Fabbro, C., Celussi, M., Russell, H., & Del Negro, P. (2012). Phenotypic and genetic diversity of coexisting Listonella anguillarum, Vibrio harveyi and Vibrio chagassi recovered from skin haemorrhages of diseased sand smelt, Atherina boyeri, in the Gulf of Trieste (NE Adriatic Sea). Letters in applied microbiology, 54(2), 153-159.https://doi.org/10.1111/j.1472-765X.2011.03188.x
• Han, Z., Sun, J., Jiang, B., Hu, X., Lv, A., Chen, L., & Guo, Y. (2021). Concurrent infections of Aeromonas veronii and Vibrio cholerae in koi carp (Cyprinus carpio var. koi). Aquaculture, 535, 736395. https://doi.org/10.1016/j.aquaculture.2021.736395
• Ina-Salwany, M. Y., Al-Saari, N., Mohamad, A., Mursidi, F. A., Mohd-Aris, A., Amal, M., Kasai, H., Mino, S., Sawabe, T., & Zamri-Saad, M. (2019). Vibriosis in Fish: A Review on Disease Development and Prevention. Journal of Aquatic Animal Health, 31(1), 3-22. https://doi.org/10.1002/aah.10045
• Ishimaru, K., Akagawa-Matsushita, M., & Muroga, K. (1996). Vibrio ichthyoenteri sp. nov., a pathogen of Japanese flounder (Paralichthys olivaceus) larvae. International Journal of Systematic and Evolutionary Microbiology, 46(1), 155-159. https://doi.org/10.1099/00207713-46-1-155
• Jahangiri, L., Shinn, A. P., Pratoomyot, J., & Gomes, G. B. (2021). Unveiling associations between ciliate parasites and bacterial microbiomes under warm-water fish farm conditions – a review. Reviews in Aquaculture, 13(2):1097–1118. https://doi.org/10.1111/raq.12514
• Jansson, E., Haenen, O., Nonnemann, B., Madsen, L., Van Gelderen, E., Aspan, A., Saker, E., Boonstra, M., Gulla, S., Colquhoun, D. J., Roozenburg-Hengst, I., & Dalsgaard, I. (2020). MALDI-TOF MS: A diagnostic tool for identification of bacterial fish pathogens. Bulletin of the European Association of Fish Pathologists, 40(6), 240–248.
• Karasu Benli, A. C., & Yavuzcan Yildiz, H. (2004). Blood parameters in Nile tilapia (Oreochromis niloticus L.) spontaneously infected with Edwardsiella tarda. Aquaculture Research, 35(14), 1388-1390. https://doi.org/10.1111/j.1365-2109.2004.01158.x
• Kotob, M. H., Menanteau-Ledouble, S., Kumar, G., Abdelzaher, M., and El-Matbouli, M. (2016). The impact of co-infections on fish: a review. Veterinary Research, 47(1), 1–12. https://doi.org/10.1186/s13567-016-0383-4
• Li, Y., Jiang, B., Mo, Z., Li, A., & Dan, X. (2022). Cryptocaryon irritans (Brown, 1951) is a serious threat to aquaculture of marine fish. Reviews in Aquaculture, 14, 218-236. https://doi.org/10.1111/raq.12594
• Ma, R., Ni, B., Fan, X., Warren, A., Yin, F., & Gu, F. (2016). Ultrastructure observation on the cells at different life history stages of Cryptocaryon irritans (Ciliophora: Prostomatea), a parasitic ciliate of marine fishes. Parasitology, 143(11), 1479-1489. https://doi.org/10.1017/S0031182016001074
• Mohamad, N., Mohd Roseli, F. A., Azmai, M. N. A., Saad, M. Z., Yasin, I. S. Md, Zulkiply, N. A., & Nasruddin, N. S. (2019). Natural concurrent infection of Vibrio harveyi and V. alginolyticus in cultured hybrid groupers in Malaysia. Journal of Aquatic Animal Health, 31(1), 88-96. https://doi.org/10.1002/aah.10055
• Mougin, J., Flahaut, C., Roquigny, R., Bonnin-Jusserand, M., Grard, T., & Le Bris, C. (2020). Rapid Identification of Vibrio Species of the Harveyi Clade Using MALDI-TOF MS Profiling With Main Spectral Profile Database Implemented With an In-House Database: Luvibase. Frontiers in Microbiology, 11(October). https://doi.org/10.3389/fmicb.2020.586536
• Moussa, M., Cauvin, E., Le Piouffle, A., Bidault, A., Paillard, C., Benoit, F., Thuillier, B., Treilles, M., Travers, M. A., & Garcia, C. (2021). A MALDI-TOF MS database for fast identification of Vibrio spp. potentially pathogenic to marine mollusks. Applied Microbiology and Biotechnology, 105(6), 2527-2539. https://doi.org/10.17882/75416
• Muniesa, A., Basurco, B., Aguilera, C., Furones, D., Reverté, C., Sanjuan‐Vilaplana, A., Jansen, M. D., Brun, E., & Tavornpanich, S. (2020). Mapping the knowledge of the main diseases affecting sea bass and sea bream in Mediterranean. Transboundary and Emerging Diseases, 67(3), 1089-1100. https://doi.org/10.1111/tbed.13482
• Nagasawa, K. & Cruz-Lacierda, E. R. (2004). Diseases of cultured groupers: Southeast Asian Fisheries Development Center. Aquaculture. Department Iloilo Philipp.
• Osthoff, M., Gürtler, N., Bassetti, S., Balestra, G., Marsch, S., Pargger, H., Weisser, M., & Egli, A. (2017). Impact of MALDI-TOF-MS-based identification directly from positive blood cultures on patient management: a controlled clinical trial, Clinical Microbiology and Infection, 23 (2), 78-85. https://doi.org/10.1016/j.cmi.2016.08.009
• Qiao, Y., Wang, J., Mao, Y., Liu, M., Chen, R., Su, Y., Ke, Q., Han, K., & Zheng, W. (2017). Pathogenic bacterium Vibrio harveyi: an endosymbiont in the marine parasitic ciliate protozoan Cryptocaryon irritans. Acta Oceanologica Sinica, 36(10), 115–119. https://doi.org/10.1007/s13131-017-1050-y
• Rivas, A. J., Lemos, M. L., & Osorio, C. R. (2013). Photobacterium damselae subsp. damselae, a bacterium pathogenic for marine animals and humans. Frontiers in Microbiology, 4, 283. https://doi.org/10.3389/fmicb.2013.00283
• Snieszko, S. F. (1974). The effects of environmental stress on outbreaks of infectious diseases of fishes. Journal of Fish Biology, 6(2), 197-208. https://doi.org/10.1111/j.1095-8649.1974.tb04537.x
• Sogawa, K., Watanabe, M., Sato, K., Segawa, S., Ishii, C., Miyabe, A., Murata, S., Saito, T., & Nomura, F. (2011). Use of the MALDI BioTyper system with MALDI-TOF mass spectrometry for rapid identification of microorganisms. Analytical and Bioanalytical Chemistry, 400(7), 1905-1911. https://doi.org/10.1007/s00216-011-4877-7
• Stentiford G. D, Sritunyalucksana, K., Flegel, T. W., Williams, B. A., Withyachumnarnkul, B., Itsathitphaisarn, O., & Bass, D. (2017). New Paradigms to Help Solve the Global Aquaculture Disease Crisis. PLoS Pathogens, 13(2), 1006160. https://doi.org/10.1371/journal.ppat.1006160 Svobodova, Z., Machova, J., Kroupova, H. K., & Velisek, J. (2017). Water Quality–Disease Relationship on Commercial Fish Farms. In G. Jeney (Ed), Fish Diseases, (Pp 167-185), Academic Press, https://doi.org/10.1016/B978-0-12-804564-0.00007-7
• Tanrikul, T., & Gultepe, N. (2011). Mix Infections in Rainbow Trout (Oncorhynchus mykiss Walbaum): Lactococcus garvieae and Vibrio anguillarum O1. Journal of Animal and Veterinary Advances. DOI: 10.3923/javaa.2011.1019.1023 Tsang, H. H., Domingos, J. A., Westaway, J. A. F., Kam, M. H. Y., Huerlimann, R., & Bastos Gomes, G. (2021). Digital droplet PCR-based environmental DNA tool for monitoring Cryptocaryon irritans in a marine fish farm from Hong Kong. Diversity, 13(8), 350. https://doi.org/10.3390/d13080350
• Turgay, E., Yardimci, R. E., & Karatas, S. (2018). First Case of Vibriosis Caused by Vibrio harveyi in Salema (Sarpa salpa) from a Public Aquarium. Süleyman Demirel Üniversitesi Eğirdir Su Ürünleri Fakültesi Dergisi 14(3), 166-172. DOI: 10.22392/egirdir.371581
• Vayssier-Taussat, M., Albina, E., Citti, C., Cosson, J. F., Jacques, M. A., Lebrun, M. H., Le Loir, Y., Ogliastro, M., Petit, M., Roumagnac, P., Candresse, T. (2014). Shifting the paradigm from pathogens to pathobiome new concepts in the light of meta-omics. Frontiers in Cellular and Infection Microbiology, 5(MAR), 1–7. https://doi.org/10.3389/fcimb.2014.00029
• Vendramin, N., Zrncic, S., Padrós, F., Oraic, D., Le Breton, A., Zarza, C., & Olesen, N. J. (2016). Fish health in Mediterranean Aquaculture, past mistakes and future challenges. Bulletin of the European Association of Fish Pathologists, 36(1), 38-45.
• Wise, A. L., LaFrentz, B. R., Kelly, A. M., Khoo, L. H., Xu, T., Liles, M. R., & Bruce, T. J. (2021). A Review of Bacterial Co-Infections in Farmed Catfish: Components, Diagnostics, and Treatment Directions. Animals, 11(11), 3240. https://doi.org/10.3390/ani11113240
• Zhang, Z., Yu, Y. X., Wang, Y. G., Liu, X., Wang, L. F., Zhang, H., Liao, M. J., & Li, B. (2020). Complete genome analysis of a virulent Vibrio scophthalmi strain VSc190401 isolated from diseased marine fish half-smooth tongue sole, Cynoglossus semilaevis. BMC Microbiology, 20(1), 1-13