DOI QR코드

DOI QR Code

Comparison of gut microbiota composition of farmed olive flounder (Paralichthys olivaceus)

  • Su-Jeong Lee (Department of Biopharmaceutical Engineering, Dong-eui University) ;
  • Young-Sun Lee (Department of Biopharmaceutical Engineering, Dong-eui University) ;
  • Tae-Rim Kim (Department of Biopharmaceutical Engineering, Dong-eui University) ;
  • Eun-Woo Lee (Department of Biopharmaceutical Engineering, Dong-eui University) ;
  • Won Je Jang (Department of Biopharmaceutical Engineering, Dong-eui University)
  • Received : 2024.02.14
  • Accepted : 2024.04.12
  • Published : 2024.08.31

Abstract

The strategy of cultivating healthy fish by manipulating their gut microbiota composition using probiotics is crucial for establishing sustainable fish farms. Information on the gut microbiota composition of healthy fish is important for the efficient development of probiotics and the aquaculture strategies that would apply them. This study assessed the gut microbiota composition of farmed olive flounder according to the growth stage to provide useful information for the development of probiotics. The fish were classified according to their weight, and the intestines of five juveniles weighing less than 100 g and five subadults weighing between 400 and 800 g were used for analysis. The results of alpha diversity analysis confirmed higher richness and diversity in the subadult group than in the juvenile group. Beta diversity analysis revealed clear boundaries and distances between the groups; however, individuals within each group were similar. The two groups showed marked differences in their gut microbiota composition. Phylum-level analysis revealed that the most abundant phylum was Proteobacteria in the juvenile group and Firmicutes in the subadult group. Notably, genus-level analysis revealed that Vibrio accounted for more than 50% of the total composition in the juvenile group. Linear discriminant analysis effect size revealed that the genera Vibrio, Photobacterium, and Leuconostoc were representative of the juvenile group, whereas 19 genera, including Lactococcus and Vagococcus, were representative of the subadult group. Thus, information on the representative microorganisms abundantly present in the intestines of healthy olive flounder can be considered for the selection and development of a probiotic genus for olive flounder farming.

Keywords

Acknowledgement

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2021R1I1A1A01049238).

References

  1. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852-7. https://doi.org/10.1038/s41587-019-0209-9
  2. Brugman S, Liu KY, Lindenbergh-Kortleve D, Samsom JN, Furuta GT, Renshaw SA, et al. Oxazolone-induced enterocolitis in zebrafish depends on the composition of the intestinal microbiota. Gastroenterology. 2009;137:1757-67. https://doi.org/10.1053/j.gastro.2009.07.069
  3. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581-3. https://doi.org/10.1038/nmeth.3869
  4. Cathers HS, Mane SP, Tawari NR, Balakuntla J, Plata G, Krishnamurthy M, et al. In silico, in vitro and in vivo characterization of host-associated Latilactobacillus curvatus strains for potential probiotic applications in farmed Atlantic salmon (Salmo salar). Sci Rep. 2022;12:18417.
  5. Chong J, Liu P, Zhou G, Xia J. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc. 2020;15:799-821. https://doi.org/10.1038/s41596-019-0264-1
  6. Egerton S, Culloty S, Whooley J, Stanton C, Paul Ross R. The gut microbiota of marine fish. Front Microbiol. 2018;9:873.
  7. Food and Agriculture Organization of the United Nations [FAO] / World Health Organization [WHO]. Evaluation of health and nutritional properties of probiotics in food including powder milk with live acid bacteria. Cordoba: Joint FAO/ WHO Expert Consultation; 2001.
  8. Hasan MT, Jang WJ, Kim H, Lee BJ, Kim KW, Hur SW, et al. Synergistic effects of dietary Bacillus sp. SJ-10 plus β-glucooligosaccharides as a synbiotic on growth performance, innate immunity and streptococcosis resistance in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2018;82:544-53. https://doi.org/10.1016/j.fsi.2018.09.002
  9. Illumina I. 16S Metagenomic sequencing library preparation: preparing 16S ribosomal RNA gene amplicons for the illumina MiSeq system. San Diego, CA: Illumina; 2013.
  10. Jang WJ, Hasan MT, Lee BJ, Hur SW, Lee S, Kim KW, et al. Effect of dietary differences on changes of intestinal microbiota and immune-related gene expression in juvenile olive flounder (Paralichthys olivaceus). Aquaculture. 2020;527:735442.
  11. Jang WJ, Jeon MH, Lee SJ, Park SY, Lee YS, Noh DI, et al. Dietary supplementation of Bacillus sp. PM8313 with β-glucan modulates the intestinal microbiota of red sea bream (Pagrus major) to increase growth, immunity, and disease resistance. Front Immunol. 2022;13:960554.
  12. Jang WJ, Lee JM, Tawheed Hasan M, Lee BJ, Lim SG, Kong IS. Effects of probiotic supplementation of a plant-based protein diet on intestinal microbial diversity, digestive enzyme activity, intestinal structure, and immunity in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2019;92:719-27. https://doi.org/10.1016/j.fsi.2019.06.056
  13. Jang WJ, Lee KB, Jeon MH, Lee SJ, Hur SW, Lee S, et al. Characteristics and biological control functions of Bacillus sp. PM8313 as a host-associated probiotic in red sea bream (Pagrus major) aquaculture. Anim Nutr. 2023;12:20-31.
  14. Jang WJ, Lee SJ, Jeon MH, Kim TY, Lee JM, Hasan MT, et al. Characterization of a Bacillus sp. KRF-7 isolated from the intestine of rockfish and effects of dietary supplementation with mannan oligosaccharide in rockfish aquaculture. Fish Shellfish Immunol. 2021;119:182-92. https://doi.org/10.1016/j.fsi.2021.09.039
  15. Jang WJ, Oh DN, Lee EJ, Lee JM. Encapsulation of probiotics with poly-γ-glutamic acid alters gut microbiota and shortchain fatty acid content by maintaining cell viability in the gastrointestinal tract. Food Hydrocoll. 2024;147:109328.
  16. Kader MA, Zahidah Azahar N, Iehata S, Bulbul M, Islam MM, Sarker J, et al. Dietary supplementation of host-associated lactic acid bacteria modulates growth, metabolic activities, and immune-related gene expression in giant freshwater prawn, Macrobrachium rosenbergii. J World Aquac Soc. 2021;52:216-30. https://doi.org/10.1111/jwas.12734
  17. Kostic AD, Howitt MR, Garrett WS. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 2013;27:701-18. https://doi.org/10.1101/gad.212522.112
  18. Lee SJ, Noh DI, Lee YS, Hasan MT, Hur SW, Lee S, et al. Effects of host-associated low-temperature probiotics in olive flounder (Paralichthys olivaceus) aquaculture. Sci Rep. 2024;14:2134.
  19. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Stephen Bircher J, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647-51. https://doi.org/10.1126/science.1155725
  20. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022-3. https://doi.org/10.1038/4441022a
  21. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489:231-41. https://doi.org/10.1038/nature11551
  22. McFall-Ngai M. Adaptive immunity: care for the community. Nature. 2007;445:153.
  23. Monroig O, Tocher DR, Navarro JC. Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs. 2013;11:3998-4018. https://doi.org/10.3390/md11103998
  24. Nawaz A, Javaid AB, Irshad S, Hoseinifar SH, Xiong H. The functionality of prebiotics as immunostimulant: evidences from trials on terrestrial and aquatic animals. Fish Shellfish Immunol. 2018;76:272-8. https://doi.org/10.1016/j.fsi.2018.03.004
  25. Nayak SK. Probiotics and immunity: a fish perspective. Fish Shellfish Immunol. 2010;29:2-14. https://doi.org/10.1016/j.fsi.2010.02.017
  26. Niu KM, Lee BJ, Kothari D, Lee WD, Hur SW, Lim SG, et al. Dietary effect of low fish meal aquafeed on gut microbiota in olive flounder (Paralichthys olivaceus) at different growth stages. MicrobiologyOpen. 2020;9:e992.
  27. Sanches-Fernandes GMM, Sa-Correia I, Costa R. Vibriosis outbreaks in aquaculture: addressing environmental and public health concerns and preventive therapies using gilthead seabream farming as a model system. Front Microbiol. 2022;13:904815.
  28. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
  29. Statistics Korea. The current fish culture by city & province, ward & county, by culture type by species [Internet]. 2024 [cited 2024 Feb 2]. https://kosis.kr/statHtml/statHtml.do?orgId=101&tblId=DT_1EZ0008&vw_cd=MT_ZTITLE&list_id=K2_4&scrId=&seqNo=&lang_mode=ko&obj_var_id=&itm_id=&conn_path=MT_ZTITLE&path=%252FstatisticsList%252FstatisticsListIndex.do
  30. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480-4. https://doi.org/10.1038/nature07540
  31. Van Doan H, Hoseinifar SH, Ringo E, Angeles Esteban M, Dadar M, Dawood MAO, et al. Host-associated probiotics: a key factor in sustainable aquaculture. Rev Fish Sci Aquac. 2020;28:16-42. https://doi.org/10.1080/23308249.2019.1643288