Abstract
Tilapia, a valuable fish species, ranks as the world’s second-largest farmed fish. In Thailand, it is a prominent cultured species, specifically the red tilapia hybrids (Oreochromis spp.). Understanding the factors influencing tilapia’s microbiome is essential to mitigate fish mortality and production decline. The study assesses the rearing water and fish gill microbiome in red tilapia culture, comparing closed earthen pond and open river cage culture systems across five provinces in Central Thailand. We conducted 16S rRNA amplicon sequencing (V3-V4 hypervariable regions) on bacterial DNA from 30 gills and 27 rearing water samples The results revealed that the location had a more significant impact (p < 0.05) than the culture system on both gills and water microbiomes. No association between abiotic factors and gill microbiome diversity was observed, while significant associations were observed between the water microbiome with ambient temperature (Ta) (p < 0.00), water temperature (Tw) (p < 0.00), pH (p < 0.03), and salinity (p < 0.01). Fish pathogens such as Streptococcus agalactiae and Mycobacterium spp. were consistently among the top 5 most abundant bacteria found in both water and fish gill samples across all provinces. Furthermore, several significant fish pathogens, including Vibrio spp., Aeromonas hydrophila, Flavobacterium spp., and Edwardsiella spp., which pose a threat to public health and food safety and security, were detected, albeit in relatively low abundance (< 0.04%). In summary, this study has identified several bacterial species present in both rearing water and red tilapia gills, some of which can cause human disease as well. Interestingly, the culture system did not have a significant impact on microbial diversity, while the farm’s location played a significant role. Further investigations into other factors such as farming practices and environmental conditions that may contribute to the presence of pathogenic bacteria in both rearing water and gill samples are warranted.
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References
Abu-Elala NM, Abd-Elsalam RM, Younis NA (2020) Streptococcosis, Lactococcosis and Enterococcosis are potential threats facing cultured Nile tilapia (Oreochomis niloticus) production. Aquac Res 51(10):4183–4195. https://doi.org/10.1111/are.14760
Amal MNA, Koh CB, Nurliyana M, Suhaiba M, Nor-Amalina Z, Santha S, Diyana-Nadhirah KP, Yusof MT, Ina-Salwany MY, Zamri-Saad M (2018) A case of natural co-infection of lilapia lake virus and Aeromonas veronii in a Malaysian red hybrid tilapia (Oreochromis niloticus×O. mossambicus) farm experiencing high mortality. Aquaculture 485:12–16
Amer A, Hamdy B, Mahmoud D, Elanany M, Rady MH, Alahmadi T, Sulaiman A, Al-Ashaal S (2021) Antagonistic activity of bacteria isolated from the Periplaneta americana L. gut against some multidrug-resistant human pathogens. Antibiotics 10(3):294–294. https://doi.org/10.3390/antibiotics10030294
ASEAN (2020) ASEAN Good Aquaculture Practices for Food Fish – trainers’ guide. Jakarta, Indonesia: ASEAN Secretariat
AVMA (2020) Guidelines for the euthanasia of animals: 2020 edition. 1931 N. Meacham Road, Schaumburg
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6(1):1–17
Bolyen E, Rideout J R, Dillon M R, Bokulich N A, Abnet C C, Al-Ghalith G A, ... & Caporaso J G (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37: 852–857. https://doi.org/10.1038/s41587-019-0209-9.
Britannica (2024) Salinity | definition, ocean, unit, examples, & facts. In Encyclopædia Britannica. Retrieved from https://www.britannica.com/science/salinity
Burbano-Gallardo E, Duque-Nivia G, Imués-Figueroa M A, Gonzalez-Legarda E, Delgado-Gómez M, Pantoja-Díaz J (2021) Effect of fish farming on sediments and the proliferation of nitrifying bacterial communities in Lake Guamuez, Colombia. Ciencia y Tecnología Agropecuaria 22(2)
Cadmus P, Brinkman SF, May MK (2018) Chronic toxicity of ferric iron for North American aquatic organisms: derivation of a chronic water quality criterion using single species and mesocosm data. Arch Environ Contam Toxicol 74(4):605–615. https://doi.org/10.1007/s00244-018-0505-2
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13(7):581–583
Chantarasiri A (2020) Diversity of cellulolytic bacteria isolated from a freshwater wetland reserve in Thailand and their cellulolytic activity. Appl Ecol Environ Res 18(4):5965–5983
Chinfak N, Charoenpong C, Somphongchaiyakul P, Wu Y, Supcharoen R, Zhang J (2023) Environmental factors influencing the distribution of fecal coliform bacteria in Bandon Bay, Thailand. Regional Studies in Marine Science: 103277–103277. https://doi.org/10.1016/j.rsma.2023.103277
Clinton M, Wyness AJ, Martin SA, Brierley AS, Ferrier DE (2021) Sampling the fish gill microbiome: a comparison of tissue biopsies and swabs. BMC Microbiol 21(1):1–15. https://doi.org/10.1186/s12866-021-02374-0
Cunillera-Montcusí D, Beklioğlu M, Cañedo-Argüelles M, Jeppesen E, Ptacnik R, Amorim CA, Arnott SE, Berger SA, Brucet S, Dugan HA, Gerhard M, Horvath Z, Langenheder S, Nejstgaard JC, Reinikainen M, Striebel M, Urrutia-Cordero P, Vad CF, Zadereev E, Matias M (2022) Freshwater salinisation: a research agenda for a saltier world. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2021.12.005
Decano EA, Templonuevo RMC, Vera Cruz EM (2020) Morphological and physiological changes in red tilapia (Oreochromis spp.) subjected to high temperature and confinement stress. Egypt Acad J Biol Sci B. Zool 12(2):103–110
Decostere A, Hermans K, Haesebrouck F (2004) Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet Microbiol 99(3–4):159–166. https://doi.org/10.1016/j.vetmic.2003.07.011
Dong HT, Techatanakitarnan C, Jindakittikul P, Thaiprayoon A, Taengphu S, Charoensapsri W, Khunrae P, Rattanarojpong T, Senapin S (2017) Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). J Fish Dis 40(10):1395–1403
Edwards P, Zhang W, Belton B, Little DC (2019) Misunderstandings, myths and mantras in aquaculture: its contribution to world food supplies has been systematically over reported. Mar Policy 106:103547. https://doi.org/10.1016/j.marpol.2019.103547
Eissa NME, El-Ghiet EA, Shaheen AA, Abbass A (2010) Characterization of Pseudomonas species isolated from tilapia “Oreochromis niloticus” in Qaroun and Wadi-El-Rayan lakes. Egypt Glob Vet 5(2):116–121
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10
FAO (2002) World fisheries and aquaculture; Food and Agriculture Organization of the United Nations: Rome, Italy; ISBN 9789251326923
FAO (2020) Fisheries and aquaculture national aquaculture sector overview - Thailand. https://www.fao.org/3/ca9229en/online/ca9229en.html
FAO (2021) FAO yearbook. Fishery and aquaculture statistics 2019/FAO annuaire. Statistiques des pêches et de l’aquaculture 2019/FAO anuario. Estadísticas de pesca y acuicultura 2019. Rome/Roma
Fracalossi DM, Turchini GM (2022) Tilapia. Reviews in aquaculture. Wiley Online Library. https://doi.org/10.1111/(ISSN)1753-5131.Tilapia
Iliyasu A, Mohamed ZA, Terano R (2016) Comparative analysis of technical efficiency for different production culture systems and species of freshwater aquaculture in Peninsular Malaysia. Aquac Rep 3:51–57. https://doi.org/10.1016/j.aqrep.2015.12.001
Infante-Villamil S, Huerlimann R, Jerry DR (2020) Microbiome diversity and dysbiosis in aquaculture. Rev Aquac 13(2):1077–1096. https://doi.org/10.1111/raq.12513
Janssen S, McDonald D, Gonzalez A, Navas-Molina JA, Jiang L, Xu ZZ, Winker K, Kado DM, Orwoll E, Manary M, Mirarab S, Knight R (2018) Phylogenetic placement of exact amplicon sequences improves associations with clinical information. Msystems 3(3):e00021-e118. https://doi.org/10.1128/mSystems.00021-18
Kanchan CM, Imjai P, Kanchan N, Panchai K (2020) Occurrence of parasitic and bacterial diseases in Thai freshwater fish. J Agric Crop Resh 8:210–214
Kim P S, Shin N R, Lee J B, Kim M S, Whon T W, Hyun D W, ... Bae J W (2021) Host habitat is the major determinant of the gut microbiome of fish. Microbiome 9(1): 166. https://doi.org/10.1186/s40168-021-01113-x
Koppang E O, Kvellestad A, Fischer U (2015) Fish mucosal immunity: gill, Editor(s): Benjamin H. Beck, Eric Peatman, Editor(s): Benjamin H. Beck, Eric Peatman, Mucosal health in aquaculture,Academic Press,Pages 93–133,ISBN 9780124171862, https://doi.org/10.1016/B978-0-12-417186-2.00005-4
Kuang T, He A, Lin Y, Huang X, Liu L (2020) Comparative analysis of microbial communities associated with the gill, gut, and habitat of two filter-feeding fish. Aquac Rep 18:10050
Lorgen-Ritchie M, Clarkson M, Chalmers L, Taylor JF, Migaud H, Martín S (2022) Temporal changes in skin and gill microbiomes of Atlantic salmon in a recirculating aquaculture system – why do they matter? Aquaculture 558:738352–738352. https://doi.org/10.1016/j.aquaculture.2022.738352
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235
Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73(5):1576–1585
Luan Y, Li M, Zhou W, Yao Y, Yang Y, Zhang Z, Ringø E, Olsen RE, Clarke JL, Xie S, Mai K, Ran C, Zhou Z (2023) The fish microbiota: research progress and potential applications. Engineering. https://doi.org/10.1016/j.eng.2022.12.011
Makori AJ, Abuom PO, Kapiyo R, Anyona DN, Dida GO (2017) Effects of water physico-chemical parameters on tilapia (Oreochromis niloticus) growth in earthen ponds in Teso North Sub-County, Busia County. Fish Aquatic Sci 20(1). https://doi.org/10.1186/s41240-017-0075-7
Marine Environment Division, Water Quality Management Bureau (2020) Marine water quality standard. EcoThailand. https://ecothailand.org/wp-content/uploads/2020/10/MrnQuaStd-1.pdf
McMurtrie J, Alathari S, Chaput D L, Bass D, Ghambi C, Nagoli J, ... & Tyler CR (2022) Relationships between pond water and tilapia skin microbiomes in aquaculture ponds in Malawi. Aquaculture 558: 738367
Merrifield DL, Rodiles A (2015) The fish microbiome and its interactions with mucosal tissues. Editor(s): Benjamin H. Beck, Eric Peatman, Mucosal health in aquaculture, Academic Press (pp. 273–295)
Minich JJ, Petrus S, Michael JD, Michael TP, Knight R, Allen EE (2020) Temporal, environmental, and biological drivers of the mucosal microbiome in a wild marine fish Scomber japonicus. Msphere 5(3):e00401-20
Minich JJ, Härer A, Vechinski J, Frable BW, Skelton ZR, Kunselman E, Shane MA, Perry DS, González A, McDonald D, Knight R, Michael TP, Allen EE (2022) Host biology, ecology and the environment influence microbial biomass and diversity in 101 marine fish species. Nat Commun 13(1). https://doi.org/10.1038/s41467-022-34557-2
Mishra A, Nam G-H, Gim J-A, Lee H-E, Jo A, Kim H-S (2018) Current challenges of streptococcus infection and effective molecular, cellular, and environmental control methods in aquaculture. Mol Cells 41(6):495–505. https://doi.org/10.14348/molcells.2018.2154
Mugwanya M, Dawood MAO, Kimera F, Sewilam H (2022) Anthropogenic temperature fluctuations and their effect on aquaculture: a comprehensive review. Aquac Fish 7(3):223–243. https://doi.org/10.1016/j.aaf.2021.12.005
Murray JL, Connell JL, Stacy A, Turner KH, Whiteley M (2014) Mechanisms of synergy in polymicrobial infections. J Microbiol 52(3):188–199. https://doi.org/10.1007/s12275-014-4067-3
Mwachiro EC, Makilla D, Bett DK, Ndeje GK (2012) A comparative study of cage and earthen pond culture of Oreochromis jipe, in Lake Jipe, Taita/Taveta District, Kenya. Retrieved from: https://docslib.org/doc/8958539/a-comparative-study-of-cage-and-earthen-pond-culture-of-oreochromis-jipe-in-lake-jipe-taita-taveta-district-kenya
Novoslavskij A, Terentjeva M, Eizenberga I, Valciņa O, Vadims B, Bērziņš A (2015) Major foodborne pathogens in fish and fish products: a review. Ann Microbiol 66(1):1–15. https://doi.org/10.1007/s13213-015-1102-5
Oetama VSP, Hennersdorf P, Abdul-Aziz MA, Mrotzek G, Haryanti H, Saluz HP (2016) Microbiome analysis and detection of pathogenic bacteria of Penaeus monodon from Jakarta Bay and Bali. Mar Pollut Bull 110(2):718–725. https://doi.org/10.1016/j.marpolbul.2016.03.043
Parrao CG, Shisler S, Moratti M, Snilstveit B (2021) Aquaculture for improving productivity, income, nutrition and women’s empowerment in low- and middle-income countries: a systematic review and meta-analysis. Campbell Syst Rev. https://doi.org/10.1002/cl2.1195
Pradeepkiran JA (2019) Aquaculture role in global food security with nutritional value: a review. Transl Anim Sci 3(2):903–910. https://doi.org/10.1093/tas/txz012
Pratte ZA, Besson M, Hollman RD, Stewart FJ (2018) The gills of reef fish support a distinct microbiome influenced by host-specific factors. Appl Environ Microbiol 84(9). https://doi.org/10.1128/aem.00063-18
Qin Y, Hou J, Deng M, Liu Q, Wu C, Ji Y, He X (2016) Bacterial abundance and diversity in pond water supplied with different feeds. Sci Rep 6(1). https://doi.org/10.1038/srep35232.
Ramirez C, Romero J (2017) The microbiome of Seriola lalandi of wild and aquaculture origin reveals differences in composition and potential function. Front Microbiol 8:1844. https://doi.org/10.3389/fmicb.2017.01844
Roh H, Park J, Kim A, Kim N, Lee Y, Kim B S, ... & Kim D H (2020) Overfeeding-induced obesity could cause potential immuno-physiological disorders in rainbow trout (Oncorhynchus mykiss). Animals 10(9): 1499. https://doi.org/10.3390/ani10091499.
Rusydi A (2018) Correlation between conductivity and total dissolved solid in various type of water: a review. IOP Conf Series: Earth Envirron Sci 118(2018):012019. https://doi.org/10.1088/1755-1315/118/1/012019
Sehnal L, Brammer-Robbins E, Wormington A M, Blaha L, Bisesi J, Larkin I, ... & Adamovsky O (2021) Microbiome composition and function in aquatic vertebrates: small organisms making big impacts on aquatic animal health. Front Microbiol 12: 567408. https://doi.org/10.3389/fmicb.2021.567408.
Steiner K, Laroche O, Walker SP, Symonds JE (2022) Effects of water temperature on the gut microbiome and physiology of Chinook salmon (Oncorhynchus tshawytscha) reared in a freshwater recirculating system. Aquaculture 560:738529–738529. https://doi.org/10.1016/j.aquaculture.2022.738529
Steinum T, Sjåstad K, Falk K, Kvellestad A, Colquhoun DJ (2009) An RT PCR-DGGE survey of gill-associated bacteria in Norwegian seawater-reared Atlantic salmon suffering proliferative gill inflammation. Aquaculture 293:172–179. https://doi.org/10.1016/j.aquaculture.2009.05.006
Sun F, Wang Y, Wang C, Zhang L, Tu K, Zheng Z (2019) Insights into the intestinal microbiota of several aquatic organisms and association with the surrounding environment. Aquaculture 507:196–202
Svobodová Z, Lloyd R, Machova J (1993) Water quality and fish health. EIFAC Technical Paper. No. 54. Rome, FAO
Svobodová Z, Machova J, Kroupova H K, Velisek J (2017) Water quality–disease relationship on commercial fish farms. Elsevier EBooks, 167–185. https://doi.org/10.1016/b978-0-12-804564-0.00007-7.
Tao E (2022) Understanding the environmental implications of the microbiome of canals in Bangkok, Thailand. Scholarship @ Claremont. https://scholarship.claremont.edu/scripps_theses/1997/Marine Environment Division, Water Quality Management Bureau. (2020). Marine Water Quality Standard. EcoThailand. https://ecothailand.org/wp-content/uploads/2020/10/MrnQuaStd-1.pdf.
Tucker CS, D’Abramo LR (2008) Managing high pH in freshwater ponds. Southern Regional Aquaculture Center. 8RAC Publication No. 4604
US Environmental Protection Agency (2013) Final aquatic life ambient water quality criteria for ammonia-freshwater 2013. Notice Federal Register 78(163):52192–52194
Whickham H (2016) ggplot2: elegant graphics for data analysis. Available online: https://ggplot2.tidyverse.org
Zhang C, Zheng X, Ren X, Li Y (2019) Wang Y (2019) Bacterial diversity in gut of large yellow croaker Larimichthys crocea and black sea bream Sparus macrocephalus reared in an inshore net pen. Fish Sci 85:1027–1036. https://doi.org/10.1007/s12562-019-01349-5
Acknowledgements
The authors would like to thank the technical support from all of the colleagues from the Center of Excellence in Fish Infectious Diseases (CE FID), Faculty of Veterinary Science, Chulalongkorn University (Bangkok, Thailand).
Funding
G.B.D. received a scholarship from the Graduate School, Chulalongkorn University the 90th Anniversary of Chulalongkorn University Fund (Ratchadapisek Somphot Endowment Fund). M.M. received a senior postdoctoral fellowship supported by Ratchadapisek Somphot from the Graduate School, Chulalongkorn University, Thailand. This project was funded by the National Research Council of Thailand (NRCT) under Mid-Career Talented Researchers Grant no. NRCT5-RSA63001-01 and Thailand Science Research and Innovation Fund Chulalongkorn University (FF67_4709668).
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G.B.D., S.C., and C.R. conceived and designed the experiments. G.B.D. and M.M. contributed equally, and C.R. performed the experiments. G.B.D., M.M., S.C., and C.R. analyzed the data and drafted the manuscript. G.B.D., M.M., C.R., and S.C. were responsible for writing, reviewing, and editing. All authors have read and agreed to the published version of the manuscript.
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Dayrit, G.B., Mabrok, M., Chaiyapechara, S. et al. Bacterial community diversity, abundance, and composition of rearing water and red tilapia gills from open river cages and earthen ponds in Central Thailand. Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01527-y
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DOI: https://doi.org/10.1007/s10499-024-01527-y