Short-term changes in microbial communities in the water column around the fish farm in the Bay of Piran


  • Valentina Turk
  • Tinkara Tinta



aquaculture, bacterial abundance, bacterial community composition, bacterial production, fluorescent in situ hybridisation, pollution


A multidisciplinary approach was used to study the impact of fish farming on coastal bacterial communities in the inner part of the Bay of Piran (northern Adriatic). Differences in bacterial abundance, production and the occurrence of selected bacterial groups were studied in the water column around the cage and at different distances from the centre of the fish cage towards the open water, i.e., reference marine station. We also examined the effect of fish feeding on the surrounding system in a short-term in situ experiment based on the simultaneous collection of seawater samples from different locations around the fish cage before and after feeding of fish. Our study suggests that fish feeding has a moderate short-term effect on water column parameters, including bacterial abundance and production, only at a limited distance from the fish cages. The nitrifying, ammonia-oxidizing bacterial groups, as determined by the fluorescent in situ hybridization method, were represented at a higher percentage in the seawater samples in the middle and around the fish cages. β- Proteobacteria, γ-Proteobacteria and the Cytophaga-Flavobacterium group were represented to a higher percentage at sampling sites in the middle of the Bay of Piran and at the reference marine station. The Vibrio group was detected at all sampling sites. The accumulation of organically enriched fish food and waste products released
into the seawater during the short-term experiment resulted in a significant increase in particulate matter, orthophosphate and ammonium. In response to the increase in inorganic nutrients, we observed a significant increase in bacterial production, while
no significant differences were observed in bacterial abundance in such short time.


Amann, R.I., Krumholz, L., Stahl, D.A. 1990. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. Journal of Bacteriology, 172(2), 762-770. DOI:

Ape, F., Manini, E., Quero, G.M., Luna, G.M., Sarà, G., Vecchio, P., Brignoli, P., Ansferri, S., Mirto, S. 2019. Biostimulation of in situ microbial degradation processes in organically-enriched sediments mitigates the impact of aquaculture. Chemosphere, 226, 715-725. DOI:

Armstrong, S.M., Hargrave, B.T., Haya, K. 2005. Antibiotic use in finfish aquaculture: modes of action, environmental fate, and microbial resistance. In Environmental effects of marine finfish aquaculture. Edited by B.T. Hargrave. Springer Berlin Heidelberg, Berlin, Heidelberg. pp. 341-357. DOI:

Asami, H., Aida, M., Watanabe, K. 2005. Accelerated sulfur cycle in coastal marine sediment beneath areas of intensive shellfish aquaculture. Applied and Environmental Microbiology, 71(6), 2925-2933. DOI:

Austin, B., and Austin, D.A. 2016. Bacterial fish pathogens: disease of farmed and wild fish. In 6th ed. 2016. Springer International Publishing : Imprint: Springer, Cham. Azam, F., and Malfatti, F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10), 782-791. DOI:

Bissett, A., Bowman, J., Burke, C. 2006. Bacterial diversity in organically-enriched fish farm sediments: Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiology Ecology, 55(1), 48-56. DOI:

Bissett, A., Burke, C., Cook, P.L.M., Bowman, J.P. 2007. Bacterial community shifts in organically perturbed sediments. Environmental Microbiology, 9(1), 46-60. DOI:

Black, K.D. (Editor). 2001. Environmental impacts of aquaculture. In 1. publ. Sheffield Academic Pr. [u.a.], Sheffield. Bouwman, A.F., Beusen, A.H.W., Overbeek, C.C., Bureau, D.P., Pawlowski, M., Glibert, P.M. 2013.

Hindcasts and future projections of global inland and coastal nitrogen and phosphorus loads due to finfish aquaculture. Reviews in Fisheries Science, 21(2), 112-156. DOI:

Cabello, F.C., Godfrey, H.P., Tomova, A., Ivanova, L., Dölz, H., Millanao, A., Buschmann, A.H. 2013. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health: Aquacultural antimicrobial use and antimicrobial resistance. Environmental Microbiology, 15(7), 1917-1942. DOI:

Caruso, G., Genovese, L., Mancuso, M., Modica, A. 2003. Effects of fish farming on microbial enzyme activities and densities: comparison between three Mediterranean sites. Letters in Applied Microbiology, 37(4), 324-328. DOI:

Castine, S.A., Bourne, D.G., Trott, L.A., McKinnon, D.A. 2009. Sediment microbial community analysis: Establishing impacts of aquaculture on a tropical mangrove ecosystem. Aquaculture, 297(1-4), 91-98. DOI:

Christensen, P., Rysgaard, S., Sloth, N., Dalsgaard, T., Schwærter, S. 2000. Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquatic Microbial Ecology, 21, 73-84. DOI:

Dowle, E., Pochon, X., Keeley, N., Wood, S.A. 2015. Assessing the effects of salmon farming seabed enrichment using bacterial community diversity and high-throughput sequencing. FEMS Microbiology Ecology, 91(8), fiv089. DOI:

Duarte, L.N., Coelho, F.J.R.C., Cleary, D.F.R., Bonifácio, D., Martins, P., Gomes, N.C.M. 2019. Bacterial and microeukaryotic plankton communities in a semi-intensive aquaculture system of sea bass (Dicentrarchus labrax): A seasonal survey. Aquaculture, 503, 59-69. DOI:

FAO (Food and Agriculture Organization of the United Nations). 2018. The State of World Fisheries and Aquaculture. FAO, Rome. 2018.

Fodelianakis, S., Papageorgiou, N., Pitta, P., Kasapidis, P., Karakassis, I., Ladoukakis, E.D. 2014. The pattern of change in the abundances of specific bacterioplankton groups is consistent across different nutrient-enriched habitats in Crete. Applied and Environmental Microbiology, 80(13), 3784-3792. DOI:

Galand, P.E., Lucas, S., Fagervold, S.K., Peru, E., Pruski, A.M., Vétion, G., Dupuy, C., Guizien, K. 2016. Disturbance increases microbial community diversity and production in marine sediments. Frontiers in Microbiology, 7. DOI:

Garren, M., Smriga, S., Azam, F. 2008. Gradients of coastal fish farm effluents and their effect on coral reef microbes. Environmental Microbiology, 10(9), 2299-2312. DOI:

Grasshoff, K., Ehrhardt, M., Kremling, K., Almgren, T. (Editors). 1983. Methods of seawater analysis. In 2nd rev. and extended ed. Verlag Chemie, Weinheim.

Grego, M., De Troch, M., Forte, J., Malej, A. 2009. Main meiofauna taxa as an indicator for assessing the spatial and seasonal impact of fish farming. Marine Pollution Bulletin, 58(8), 1178-1186. DOI:

Grego, M., Malej, A., De Troch, M. 2020. The depleted carbon isotopic signature of nematodes and harpacticoids and their place in carbon processing in fish farm sediments. Frontiers in Marine Science, 7, 572. DOI:

Hargrave, B., Duplisea, D., Pfeiffer, E., Wildish, D. 1993. Seasonal changes in benthic fluxes of dissolved oxygen and ammonium associated with marine cultured Atlantic salmon. Marine Ecology Progress Series, 96, 249-257. DOI:

Hargrave, B.T., Phillips, G.A., Doucette, L.I., White, M.J., Milligan, T.G., Wildish, D.J., Cranston, R.E. 1997. Assessing benthic impacts of organic enrichment from marine aquaculture. Water, Air, & Soil Pollution, 99(1-4), 641-650. DOI:

Karakassis, I., Tsapakis, M., Hatziyanni, E. 1998. Seasonal variability in sediment profiles beneath fish farm cages in the Mediterranean. Marine Ecology Progress Series, 162, 243-252. DOI:

Karakassis, I. 2000. Impact of cage farming of fish on the seabed in three Mediterranean coastal areas. ICES Journal of Marine Science, 57(5), 1462-1471. DOI:

Kawahara, N., Shigematsu, K., Miyadai, T., Kondo, R. 2009. Comparison of bacterial communities in fish farm sediments along an organic enrichment gradient. Aquaculture, 287(1-2), 107-113. DOI:

Kim, S.-R., Nonaka, L., Suzuki, S. 2004. Occurrence of tetracycline resistance genes tet (M) and tet (S) in bacteria from marine aquaculture sites. FEMS Microbiology Letters, 237(1), 147-156. DOI:

Kirchman, D.L. 1994. The uptake of inorganic nutrients by heterotrophic bacteria. Microbial Ecology, 28(2), 255-271. DOI:

Kirchman, D.L. 2016. Growth rates of microbes in the oceans. Annual Review of Marine Science, 8(1), 285-309. DOI:

Kolda, A., Gavrilović, A., Jug-Dujaković, J., Ljubešić, Z., El-Matbouli, M., Lillehaug, A., Lončarević, S., Perić, L., Knežević, D., Vukić Lušić, D., Kapetanović, D. 2020. Profiling of bacterial assemblages in the marine cage farm environment, with implications on fish, human and ecosystem health. Ecological Indicators, 118, 106785. DOI:

Kondo, R., Shigematsu, K., Kawahara, N., Okamura, T., Yoon, Y.H., Sakami, T., Yokoyama, H., Koizumi, Y. 2012. Abundance of sulphate-reducing bacteria in fish farm sediments along the coast of Japan and South Korea. Fisheries Science, 78(1), 123-131. DOI:

Kovac, N., Čermelj, B., Vrišer, B., Lojen, S. 2003. Influence of fish farming on coastal marine sediment in Slovenia (Piran Bay, northern Adriatic):Final report. National Institute of Biology. Lee, S., and Fuhrman, J.A. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Applied and Environmental Microbiology, 53(6), 1298-1303. DOI:

Lojen, S., Spanier, E., Tsemel, A., Katz, T., Eden, N., Angel, D.L. 2005. δ15N as a natural tracer of particulate nitrogen effluents released from marine aquaculture. Marine Biology, 148(1), 87-96. DOI:

Luna, G.M., Corinaldesi, C., Dell’Anno, A., Pusceddu, A., Danovaro, R. 2013. Impact of aquaculture on benthic virus–prokaryote interactions in the Mediterranean Sea. Water Research, 47(3), 1156-1168. DOI:

Malačič, V., and Forte, J. 2003. Distribution of the food surplus and faecal particles on the seabed bellow a fish farm in the Bay of Piran. Annales, Series Historia Naturalis, (13), 3-8.

Malfatti, F., Turk, V., Tinta, T., Mozetič, P., Manganelli, M., Samo, T.J., Ugalde, J.A., Kovač, N., Stefanelli, M., Antonioli, M., Fonda-Umani, S., Del Negro, P., Cataletto, B., Hozić, A., Ivošević DeNardis, N., Žutić, V., Svetličić, V., Mišić Radić, T., Radić, T., Fuks, D., Azam, F. 2014. Microbial

mechanisms coupling carbon and phosphorus cycles in phosphorus-limited northern Adriatic Sea. Science of the Total Environment, 470-471, 1173-1183. DOI:

Martins, P., Coelho, F.J.R.C., Cleary, D.F.R., Pires, A.C.C., Marques, B., Rodrigues, A.M., Quintino, V., Gomes, N.C.M. 2018. Seasonal patterns of bacterioplankton composition in a semi-intensive European seabass (Dicentrarchus labrax) aquaculture system. Aquaculture, 490, 240-250. DOI:

Matijević, S., Kušpilić, G., Morović, M., Grbec, B., Bogner, B., Skejić, S., Veža, J. 2009. Physical and chemical properties of the water column and sediments at sea bass/sea bream farm in the middle Adriatic (Maslinova Bay). Acta Adriatica, (50 (1)), 59-76.

McCaig, A.E., Phillips, C.J., Stephen, J.R., Kowalchuk, G.A., Harvey, S.M., Herbert, R.A., Embley, T.M., Prosser, J.I. 1999. Nitrogen cycling and community structure of proteobacterial β-subgroup ammonia-oxidizing bacteria within polluted marine fish farm sediments. Applied and Environmental Microbiology, 65(1), 213-220. DOI:

McGhie, T.K., Crawford, C.M., Mitchell, I.M., O’Brien, D. 2000. The degradation of fish-cage waste in sediments during fallowing. Aquaculture, 187(3-4), 351-366. DOI:

Mirto, S., La rosa, T., Danovaro, R., Mazzola, A. 2000. Microbial and meiofaunal response to intensive mussel-farm biodeposition in coastal sediments of the western Mediterranean. Marine Pollution Bulletin, 40(3), 244-252. DOI:

Mirto, S., Gristina, M., Sinopoli, M., Maricchiolo, G., Genovese, L., Vizzini, S., Mazzola, A. 2012. Meiofauna as an indicator for assessing the impact of fish farming at an exposed marine site. Ecological Indicators, 18, 468-476. DOI:

Navarro, N., Leakey, R., Black, K. 2008. Effect of salmon cage aquaculture on the pelagic environment of temperate coastal waters: seasonal changes in nutrients and microbial community. Marine Ecology Progress Series, 361, 47-58. DOI:

Pitta, P., Apostolaki, E.T., Tsagaraki, T., Tsapakis, M., Karakassis, I. 2006. Fish farming effects on chemical and microbial variables of the water column: a spatio-temporal study along the Mediterranean sea. Hydrobiologia, 563(1), 99-108. DOI:

Price, C., Black, K., Hargrave, B., Morris, J. 2015. Marine cage culture and the environment: effects on water quality and primary production. Aquaculture Environment Interactions, 6(2), 151-174. DOI:

Quero, G.M., Cassin, D., Botter, M., Perini, L., Luna, G.M. 2015. Patterns of benthic bacterial diversity in coastal areas contaminated by heavy metals, polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs). Frontiers in Microbiology, 6. Reimers, C.E., Alleau, Y., Bauer, J.E., Delaney, J., Girguis, P.R., Schrader, P.S., Stecher, H.A. 2013. Redox effects on the microbial degradation of refractory organic matter in marine sediments. Geochimica et Cosmochimica Acta, 121, 582-598. DOI:

Roquigny, R., Mougin, J., Le Bris, C., Bonnin-Jusserand, M., Doyen, P., Grard, T. 2021. Characterization of the marine aquaculture microbiome: A seasonal survey in a seabass farm. Aquaculture, 531, 735987. DOI:

Šestanović, S., Peković, J., Matijević, S., Ninčević Gladan, Ž. 2016. Effects of fish farming on microbial planktonic communities in the middle Adriatic sea. Aquaculture Research, 47(4), 1040-1054. DOI:

Simon, M., and Azam, F. 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine Ecology Progress Series, 51, 201-213. DOI:

Sjöstedt, J., Pontarp, M., Tinta, T., Alfredsson, H., Turk, V., Lundberg, P., Hagström, Å., Riemann, L. 2013. Reduced diversity and changed bacterioplankton community composition do not affect utilization of dissolved organic matter in the Adriatic Sea. Aquatic Microbial Ecology, 71(1), 15-24. DOI:

Smith, D.M., and Azam, F. 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Marine Microbial Food Webs, 6, 107-114.

Štrukelj, M. 2008. Vpliv marikulture na okolje: diplomsko delo. Univerza Nova Gorica, Nova Gorica. Thompson, F.L., Austin, B.,Swings, J. (Editors). 2006. The Biology of Vibrios. ASM Press, Washington, DC, USA. Tinta, T., Vojvoda, J., Mozetič, P., Talaber, I., Vodopivec, M., Malfatti, F., Turk, V. 2015. Bacterial community shift is induced by dynamic environmental parameters in a changing coastal ecosystem (northern Adriatic, northeastern Mediterranean Sea) - a 2-year time-series study: Bacterial community shift in a dynamic coastal ecosystem. Environmental Microbiology, 17(10), 3581-3596. DOI:

Turk, V., Rehnstam, A.-S., Lundberg, E., Hagström, Å. 1992. Release of Bacterial DNA by Marine Nanoflagellates, an Intermediate Step in Phosphorus Regeneration. Applied and Environmental Microbiology, 58(11), 3744-3750. DOI:

Turk, V., and Malej, A. 2003. The influence of fish cage aquaculture on acterioplankton in the Bay of piran (Gulf of Trieste, Adriatic Sea. Annales, Series Historia Naturalis 13(1), 37-42.

Turk, V., Malkin, S., Celussi, M., Tinta, T., Cram, J., Malfatti, F., Chen, F. 2020. Ecological role of microbes: current knowledge and future prospects. In Geophysical Monograph Series, 1st edition. Edited by T.C. Malone, A. Malej, and J. Faganeli. Wiley. pp. 129-145. DOI:

Vezzulli, L., Chelossi, E., Riccardi, G., Fabiano, M. 2002. Bacterial community structure and activity in fish farm sediments of the Ligurian sea (Western Mediterranean). Aquaculture International, 10(2), 123-141. DOI:

Vezzulli, L., Moreno, M., Marin, V., Pezzati, E., Bartoli, M., Fabiano, M. 2008. Organic waste impact of capture-based Atlantic bluefin tuna aquaculture at an exposed site in the Mediterranean Sea. Estuarine, Coastal and Shelf Science, 78(2), 369-384. DOI:

Wang, X., Cuthbertson, A., Gualtieri, C., Shao, D. 2020. A Review on mariculture effluent: characterization and management tools. Water, 12(11), 2991. DOI:






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Turk, V., & Tinta, T. (2021). Short-term changes in microbial communities in the water column around the fish farm in the Bay of Piran. Acta Biologica Slovenica, 64(2), 9-23.

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