Abstract
The Korean rockfish, Sebastes schlegeli, is most commonly farmed in sea cages along the coast of Korea; however, detailed information on intestinal microbiota regarding this fish is not readily available. In this study, comparison of the seasonal changes of microbial communities in the intestine between farmed and wild through the amplicon sequencing approach was conducted. The composition of major species in the intestine of this fish was very simple compared to that of other marine fish species, with members affiliated with the family Vibrionaceae hyper-dominating and comprising on average 97.6% of microbiota. However, the composition at the genus or species level and the pattern of seasonal changes of diversity indices showed significant differences between farmed and wild fish. In the farmed fish, Photobacterium phophoreum was most dominant throughout the year, accounting for 58.8% of the total. Aliivibrio fisherii and/or Aliivibrio finisterrensis also were dominant in the fall to winter but substituted by Photobacterium damselae during spring to summer. In the wild fish, on the other hand, opportunistic pathogens in the genera Aliivibrio or Vibrio were dominant in most of the samples. The analysis of shared species between gut microbiome, feed microbiota, and seawater microbiota indicated that the intestinal microbial diversity of farmed fish was affected more by microbiota of seawater than that of feed in spring and winter seasons. Additionally, the proportion of potential pathogenic Vibrio spp. in the gut showed a negative correlation with plasma glucose levels of the host. This study and following studies will be helpful in understanding the interaction between microbiome hosts and the development of techniques to enhance production of healthy Korean rockfish.
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References
Aquilera E, Yany G, Romero J (2013) Cultivable intestinal microbiota of yellowtail juveniles (Seriola lalandi) in an aquaculture system. Lat Am J Aquat Res 41:395–403. https://doi.org/10.3856/vol41-issue3-fulltext-3
Banerjee G, Ray AK (2017) Bacterial symbiosis in the fish gut and its role in health and metabolism. Symbiosis 72:1–11
Baross J, Liston J (1970) Occurrence of Vibrio parahaemolyticus and related hemolytic vibrios in marine environments of Washington State. Appl Microbiol 20:179–186
Baticados M, Lavilla-Pitogo C, Cruz-Lacierda E, De La Pena L, Sunaz N (1990) Studies on the chemical control of luminous bacteria Vibrio harveyi and V. splendidus isolated from diseased Penaeus monodon larvae and rearing water. Dis Aquat Org 9:133–139. https://doi.org/10.3354/dao009133
Beaz-Hidalgo R, Doce A, Balboa S, Barja JL, Romalde JL (2010) Aliivibrio finisterrensis sp. nov., isolated from Manila clam, Ruditapes philippinarum and emended description of the genus Aliivibrio. Int J Syst Evol Microbiol 60:223–228. https://doi.org/10.1099/ijs.0.010710-0
Bowman JP (2006) The genus Psychrobacter. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York, pp 920–930
Choi H-S, Myoung J-I, Park M, Cho M-Y (2009) A Study on the summer mortality of Korean rockfish Sebastes schlegelii in Korea. J Fish Pathol 22:155–162 (in Korean)
Egerton S, Culloty S, Whooley J, Stanton C, Ross RP (2018) The gut microbiota of marine fish. Front Microbiol 9:873. https://doi.org/10.3389/fmicb.2018.00873
Egidius E, Andersen K, Clausen E, Raa J (1981) Cold-water vibriosis or “Hitra disease” in Norwegian salmonid farming. J Fish Dis 4:353–354. https://doi.org/10.1111/j.1365-2761.1981.tb01143.x
Egidius E, Wiik R, Andersen K, Hoff K, Hjeltnes B (1986) Vibrio salmonicida sp. nov., a new fish pathogen. Int J Syst Evol Microbiol 36:518–520. https://doi.org/10.1099/00207713-36-4-518
Farto R, Armada S, Montes M, Guisande J, Pérez M, Nieto T (2003) Vibrio lentus associated with diseased wild octopus (Octopus vulgaris). J Invertebr Pathol 83:149–156. https://doi.org/10.1016/s0022-2011(03)00067-3
Farto R, Armada S, Montes M, Perez M, Nieto T (2006) Presence of a lethal protease in the extracellular products of Vibrio splendidus–Vibrio lentus related strains. J Fish Dis 29:701–707. https://doi.org/10.1111/j.1365-2761.2006.00746.x
Gauthier G, Lafay B, Ruimy R, Breittmayer V, Nicolas J-L, Gauthier M, Christen R (1995) Small- subunit rRNA sequences and whole DNA relatedness concur for the reassignment of Pasteurella piscicida (Snieszko et al.) Janssen and Surgalla to the genus Photobacterium as Photobacterium damsela subsp. piscicida comb. nov. Int J Syst Evol Microbiol 45:139–144. https://doi.org/10.1099/00207713-45-1-139
Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154. https://doi.org/10.1111/j.1574-695X.2007.00343.x
Haygood MG (1993) Light organ symbioses in fishes. Crit Rev Microbiol 19:191–216. https://doi.org/10.3109/10408419309113529
Hyun D-W, Oh SJ, Kim M-S, Whon TW, Jung M-J, Shin N-R, Kim PS, Kim HS, Lee J-Y, Kang W, Bae JW (2015) Simplicispira piscis sp. nov., isolated from the gut of a Korean rockfish, Sebastes schlegelii. Int J Syst Evol Microbiol 65:4689–4694. https://doi.org/10.1099/ijsem.0.000635
Islam MJ, Slater MJ, Kunzmann A (2020) What metabolic, osmotic and molecular stress responses tell us about extreme ambient heatwave impacts in fish at low salinities: the case of European seabass Dicentrarchus Labrax. Sci Total Environ 749:141458. https://doi.org/10.1016/j.scitotenv.2020.141458
Iwama R, Ashida M (1986) Biosynthesis of prophenoloxidase in hemocytes of larval hemolymph of the silkworm, Bombyx mori. Insect Biochem 16:547–555. https://doi.org/10.1016/0020-1790(86)90032-6
Jiang Y, Liu X, Xu Y, Shi B, Wang B (2020) Microbiota characteristics in Sebastes schlegelii intestine in early life stages. J Oceanol Limnol 38:275–287. https://doi.org/10.1007/s00343-019-9011-2
Kang W, Kim PS, Hyun D-W, Lee J-Y, Kim HS, Oh SJ, Shin N-R, Bae J-W (2016) Comamonas piscis sp. nov., isolated from the intestine of a Korean rockfish, Sebastes schlegelii. Int J Syst Evol Microbiol 66:780–785. https://doi.org/10.1099/ijsem.0.000790
Kim B-T, Brown CL, Kim D-H (2019) Assessment on the vulnerability of Korean aquaculture to climate change. Mar Policy 99:111–122. https://doi.org/10.1016/j.marpol.2018.10.009
Lee MD, Kling JD, Araya R, Ceh J (2018) Jellyfish life stages shape associated microbial communities, while a core microbiome is maintained across all. Front Microbiol 9:1534. https://doi.org/10.3389/fmicb.2018.01534
Li J, Woo NYS (2003) Pathogenicity of vibrios in fish: An overview. J Ocean Univ Qingdao 2:117–128. https://doi.org/10.1007/s11802-003-0039-7
Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5:207. https://doi.org/10.3389/fmicb.2014.00207
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172. https://doi.org/10.1038/ismej.2010.133
Matanza XM, Osorio CR (2018) Transcriptome changes in response to temperature in the fish pathogen Photobacterium damselae subsp. damselae: clues to understand the emergence of disease outbreaks at increased seawater temperatures. PLoS ONE 13:e0210118. https://doi.org/10.1371/journal.pone.0210118
Møyner K, Røed KH, Sevatdal S, Heum M (1993) Changes in non-specific immune parameters in Atlantic salmon, Salmo salar L., induced by Aeromonas salmonicida infection. Fish Shellf Immun 3:253–265. https://doi.org/10.1006/FSIM.1993.1025
Ntranos A, Casaccia P (2018) The microbiome–gut–behavior axis: crosstalk between the gut microbiome and oligodendrocytes modulates behavioral responses. Neurotherapeutics 15:31–35. https://doi.org/10.1007/s13311-017-0597-9
Pan H, Li Z, Xie J, Liu D, Wang H, Yu D, Zhang Q, Hu Z, Shi C (2019) Berberine influences blood glucose via modulating the gut microbiome in Grass Carp. Front Microbiol 10:1066. https://doi.org/10.3389/fmicb.2019.01066
Park K-D, Kang Y-J, Huh S-H, Kwak S-N, Kim H-W, Lee H-W (2007) Feeding ecology of Sebastes schlegelii in the Tongyeong marine ranching area. Korean J Fish Aquat Sci 40:308–314. https://doi.org/10.5657/kfas.2007.40.5.308(inKorean)
Qiao G, Lee DC, Woo SH, Li H, Xu D-H, Park SI (2012) Microbiological characteristics of Vibrio scophthalmi isolates from diseased olive flounder Paralichthys olivaceus. Fisheries Sci 78:853–863. https://doi.org/10.1007/s12562-012-0502-8
Ramírez C, Romero J (2017) Fine flounder (Paralichthys adspersus) microbiome showed important differences between wild and reared specimens. Front Microbiol 8:271. https://doi.org/10.3389/fmicb.2017.00271
Rivas AJ, Lemos ML, Osorio CR (2013) Photobacterium damselae subsp. damselae, a bacterium pathogenic for marine animals and humans. Front Microbiol 4:283. https://doi.org/10.3389/fmicb.2013.00283
Romalde JL (2002) Photobacterium damselae subsp. piscicida: an integrated view of a bacterial fish pathogen. Int Microbiol 5:3–9. https://doi.org/10.1007/s10123-002-0051-6
Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Freenberg EP (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102:3004–3009. https://doi.org/10.1073/pnas.0409900102
Sayes C, Leyton Y, Riquelme C (2018) Probiotic bacteria as an healthy alternative for fish aquaculture. In: Savic S (ed) Antibiotics use in animals. InTech Publishers, London, pp 115–132. https://doi.org/10.5772/intechopen.71206
Sonh MH, Park MA, Kim JW, Kim KW, Kang YJ, Park YB, Eo YY (2007) Standard manual of black rockfish culture. National Fisheries Research and Development Institute, Busan, p 184 (in Korean)
Soto D, Ross LG, Handisyde N, Bueno PB, Beveridge MCM, Dabbadie L, Aguilar-Manjarrez J, Cai J, Pongthanapanich T (2018) Climate change and aquaculture: vulnerability and adaptation options. In: Barange M, Bahri T, Beveridge MCM, Cochrane KL, Funge-Smith S, Poulain F (eds) Impacts of climate change on fisheries and aquaculture, synthesis of current knowledge, adaptation and mitigation options. FAO, Rome, pp 465–490
Sullam KE, Essinger SD, Lozupone CA, O’CONNOR MP, Rosen GL, Knight R, Kilham SS, Russell JA, (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21:3363–3378. https://doi.org/10.1111/j.1365-294X.2012.05552.x
Tak EJ, Kim HS, Lee J-Y, Kang W, Hyun D-W, Kim PS, Shin N-R, Bae J-W (2018) Tessaracoccus aquimaris sp. nov., isolated from the intestine of a Korean rockfish, Sebastes schlegelii, from a marine aquaculture pond. Int J Syst Evol Microbiol 68:1065–1072. https://doi.org/10.1099/ijsem.0.002626
Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PLoS ONE 9:e105592. https://doi.org/10.1371/journal.pone.0105592
Tinta T, Kogovšek T, Klun K, Malej A, Herndl GJ, Turk V (2019) Jellyfish-associated microbiome in the marine environment: exploring its biotechnological potential. Mar Drugs 17:94. https://doi.org/10.3390/md17020094
Walburn JW, Wemheuer B, Thomas T, Copeland E, O’Connor W, Booth M, Fielder S, Egan S (2018) Diet and diet-associated bacteria shape early microbiome development in Yellowtail Kingfish (Seriola lalandi). Microb Biotechnol 12:275–288. https://doi.org/10.1111/1751-7915.13323
Wang AR, Ran C, Ringø E, Zhou ZG (2018) Progress in fish gastrointestinal microbiota research. Rev Aquacult 10:626–640. https://doi.org/10.1111/raq.12191
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Acknowledgements
This work was supported by the grants of KIOST In-house Program (PE99822), Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, and Forestry (IPET) through the Golden Seed Project (213008-05-4-SB420) of the Republic of Korea and MarineBiotics Project (20210469) funded by the Ministry of Ocean and Fisheris of the Republic of Korea.
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Yu, J., Kang, M.J., Kim, Y.J. et al. Comparison of Intestine Microbiota Between Wild and Farmed Korean Rockfish, Sebastes schlegelii. Ocean Sci. J. 56, 297–306 (2021). https://doi.org/10.1007/s12601-021-00022-2
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DOI: https://doi.org/10.1007/s12601-021-00022-2