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Comparison of the Intestinal Bacteria Between Black Seabass Centropristis striata Reared in Recirculating Aquaculture System and Net Pen

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Abstract

Determination of diversity and function of the bacteria in fish gut is essential to understanding the interaction between intestinal bacteria and their host organism. This study compared intestinal bacterial community of black seabass (Centropristis striata) hatched by the same breeding farm but reared in different aquaculture systems, an indoor recirculating aquaculture system (RAS) and an inshore net pen (INP). The fish were fed with formulated feed manufactured by same feed company. Bacteria in fish gut, formulated feed and seawater were identified by 16S rRNA high throughout sequencing (HTS). Total 1484 OTUs, which belonged to 34 phyla and 79 genera, were identified from fish gut, formulated feed and seawater. In fish gut, 24 phyla and 43 genera were identified. Proteobacteria, Fusobacteria, and Firmicutes dominated at the phylum level in fish gut in INP, while Proteobacteria and Firmicutes dominated in fish gut in RAS. Photobacterium, Vibrio, and Cetobacterium dominated at the genus level in fish gut in both INP and RAS. One OTU of Photobacterium occurred in all the fish gut samples, suggesting this bacterium might be the main component of the core microbiota. No significant difference was found in bacterial diversity in fish gut between INP and RAS, suggesting genetic background should be a primary factor determining intestinal bacterial community of black seabass. Bacterial diversity in seawater was high relative to that in fish gut and formulated feed, regardless in INP or RAS. The common OTU between fish gut and seawater was more than that between fish gut and formulated feed in INP, while the common OTU between fish gut and seawater was slightly less than that between fish gut and formulated feed in RAS. These results reveal that the bacteria in formulated feed and seawater could influence the bacteria in fish gut, and their priority in shaping intestinal bacterial community depended on the bacterial composition in feed and seawater. This study reveals that intestinal bacterial community of black seabass was influenced by both genetic background and environmental factors.

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Data Availability

All the sequences data can be accessed in the GSA database under the accession number CRA004279 (https://bigd.big.ac.cn/gsa/browse/CRA004279). The data can also be asked from the corresponding author.

Code Availability

The data of this study are analyzed by QIIME2, figures are plotted by ggplot2.

References

  1. O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693

    Article  PubMed  PubMed Central  Google Scholar 

  2. Cryan JF, O’Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV et al (2019) The microbiota-gut-brain axis. Physiol Rev 99:1877–2013

    Article  CAS  PubMed  Google Scholar 

  3. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Knights D, Walters WA, Peña AG, Pirrung M, Stombaugh J, Caporaso JG, Goodrich JK, Bittinger K, Lozupone CA, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed  PubMed Central  Google Scholar 

  5. Egerton S, Culloty S, Whooley J, Stanton C, Ross RP (2018) The gut microbiota of marine fish. Front Microbiol 9:873

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ou W, Yu G, Zhang Y, Mai K (2021) Recent progress in the understanding of the gut microbiota of marine fishes. Mar Life Sci Technol 3:434–448

    Article  Google Scholar 

  7. Yukgehnaish K, Kumar P, Sivachandran P, Marimuthu K, Arshad A, Paray BA, Arockiaraj J (2020) Gut microbiota metagenomics in aquaculture: factors influencing gut microbiome and its physiological role in fish. Rev Aquac 12:1903–1927

    Google Scholar 

  8. Ringø E, Zhou Z, Vecino JLG, Wadsworth S, Romero J, Krogdahl Å, Olsen RE, Dimitroglou A, Foey A, Davies S et al (2016) Effect of dietary components on the gut microbiota of aquatic animals. a never-ending story? Aquac Nutr 22:219–282

    Article  Google Scholar 

  9. Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J Appl Microbiol 123(1):2–17

    Article  CAS  PubMed  Google Scholar 

  10. Zhou Z, Ringø E, Olsen RE, Song SK (2018) Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: a review. Aquac Nutr 24:644–665

    Article  CAS  Google Scholar 

  11. Ghanbari M, Kneifel W, Domig KJ (2015) A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448:464–475

    Article  CAS  Google Scholar 

  12. Uma A, Subash P, Abraham TJ (2020) Importance of gut microbiota in fish—a review. Indian J Anim Hlth 59:181–194

    Article  Google Scholar 

  13. Blancheton JP, Attramadal KJK, Michaud L, Roque d’Orbcastel D, Vadstein O (2013) Insight into bacterial population in aquaculture systems and its implication. Aquacult Eng 53:30–39

    Article  Google Scholar 

  14. Buchan A, Lecleir GR, Gulvik CA, González JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698

    Article  CAS  PubMed  Google Scholar 

  15. Huizinga HW, Esch GW, Hazen TC (1979) Histopathology of red-sore disease (Aeromonas Hydrophila) in naturally and experimentally infected largemouth bass Micropterus Salmoides (Lacepede). J Fish Dis 2:263–277

    Article  Google Scholar 

  16. Melo Bolívar JF, Ruiz Pardo RY, Hume ME, Villamil Díaz LM (2021) Multistrain probiotics use in main commercially cultured freshwater fish: a systematic review of evidence. Rev Aquac 13(4):1758–1780.

    Article  Google Scholar 

  17. Olmos J, Acosta M, Mendoza G, Pitones V (2020) Bacillus Subtilis, an ideal probiotic bacterium to shrimp and fish aquaculture that increase feed digestibility, prevent microbial diseases, and avoid water pollution. Arch Microbiol 202:427–435

    Article  CAS  PubMed  Google Scholar 

  18. Zhang C, Zheng X, Ren X, Li Y, 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

    Article  CAS  Google Scholar 

  19. Chiarello M, Paz VI, Veyssière C, Santoul F, Loot G, Ferriol J, Boulêtreau S (2019) Environmental conditions and neutral processes shape the skin microbiome of European catfish (Silurus Glanis) populations of southwestern France. Environmental Microbiology Reports 11:605–614

    Article  PubMed  Google Scholar 

  20. Eichmiller JJ, Hamilton MJ, Staley C, Sadowsky MJ, Sorensen PW (2016) Environment shapes the fecal microbiome of invasive carp species. Microbiome 4:44–52

    Article  PubMed  PubMed Central  Google Scholar 

  21. Llewellyn MS, Mcginnity P, Dionne M, Letourneau J, Thonier F, Carvalho GR, Creer S, Derome N (2016) The biogeography of the atlantic salmon (Salmo Salar) gut microbiome. ISME J 10:1280–1284

    Article  PubMed  Google Scholar 

  22. Romero J, Ringø E, Merrifield DL (2014) The gut microbiota of fish. In: Merrifield D, Ringø E (eds) Aquaculture nutrition: gut health, probiotics and prebiotics. John Wiley & Sons, Chichester, pp 75–100

    Chapter  Google Scholar 

  23. Kokou F, Sasson G, Friedman J, Eyal S, Ovadia O, Harpaz S, Cnaani A, Mizrahi I (2019) Core gut microbial communities are maintained by beneficial interactions and strain variability in fish. Nat Microbiol 4:2456–2465

    Article  PubMed  Google Scholar 

  24. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shade A, Handelsman J (2012) Beyond the venn diagram: the hunt for a core microbiome. Environ Microbiol 14:4–12

    Article  CAS  PubMed  Google Scholar 

  26. Turnbaugh PJ, Gordon JI (2009) The core gut microbiome, energy balance and obesity. J Physiol 587:4153–4158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Anderson W, Milagrosa Bustamante G, Carpenter KE, Gilmore G, Robertson R (2015) Centropristis striata. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T16435325A16510242.en

  28. Callahan BJ, Mcmurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V et al (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–2830

    Google Scholar 

  30. Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Moeller S (2005) Gplots: various R programming tools for plotting data.https://cran.r-project.org/package=gplots

  32. Wang AR, Ran C, Ringø E, Zhou ZG (2018) Progress in fish gastrointestinal microbiota research. Rev Aquac 10:626–640

    Article  Google Scholar 

  33. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21:3100–3102

    Article  PubMed  PubMed Central  Google Scholar 

  36. Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, Kempher ML, Wu L, Wang Y, Liao L et al (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18:4739–4754

    Article  CAS  PubMed  Google Scholar 

  37. Le D, Nguyen P, Nguyen D et al (2020) Gut microbiota of migrating wild rabbit fish (Siganus guttatus) larvae have low spatial and temporal variability. Microb Ecol 79:539–551

    Article  PubMed  Google Scholar 

  38. Dehler CE, Secombes CJ, Martin SAM (2017) Environmental and physiological factors shape the gut microbiota of atlantic salmon parr (Salmo Salar L.). Aquaculture 467:149–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lauzon HL, Gudmundsdottir S, Petursdottir SK, Reynisson E, Steinarsson A, Oddgeirsson M, Bjornsdottir R, Gudmundsdottir BK (2010) Microbiota of atlantic cod (Gadus Morhua L.) rearing systems at pre-and posthatch stages and the effect of different treatments. J Appl Microbiol 109:1775–1789

    CAS  PubMed  Google Scholar 

  40. Mcintosh D, Ji B, Forward BS, Puvanendran V, Boyce D, Ritchie R (2008) Culture-independent characterization of the bacterial populations associated with cod (Gadus Morhua L.) and live feed at an experimental hatchery facility using denaturing gradient gel electrophoresis. Aquaculture 275:42–50

    Article  CAS  Google Scholar 

  41. Blanch AR, Alsina M, Simon M, Jofre J (1997) Determination of bacteria associated with reared turbot (Scophthalmus Maximus) larvae. J Appl Microbiol 82:729–734

    Article  Google Scholar 

  42. Hansen GH, Olafsen JA (1999) Bacterial interactions in early life stages of marine cold water fish. Microb Ecol 38:1–26

    Article  CAS  PubMed  Google Scholar 

  43. Giatsis C, Sipkema D, Smidt H, Verreth JAJ, Verdegem MCJ, Jiravanichpaisal P (2014) The colonization dynamics of the gut microbiota in tilapia larvae. PLoS ONE 9:e103641

    Article  PubMed  PubMed Central  Google Scholar 

  44. Tsuchiya C, Sakata T, Sugita H (2008) Novel ecological niche of Cetobacterium Somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol 46:43–48

    CAS  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (Grant No. 31772868). We thank Dr. Jingan Wang and Victor Hector for their suggestion in revising the manuscript.

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Author notes

  1. Cong Yu and Chen Zhang have contributed equally to this research.

Authors and Affiliations

  1. Ocean College, Zhejiang University, Zhoushan, 316021, Zhejiang, People’s Republic of China

    Cong Yu, Chen Zhang, Abba Salisu & Yan Wang

  2. Department of Biological Sciences, Bayero University, Kano, PMB 3011, Nigeria

    Abba Salisu

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  1. Cong Yu
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  2. Chen Zhang
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  4. Yan Wang
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Contributions

CY participated in sample collection, conducted data analysis and drafted the manuscript. CZ conducted sample collection and bacterial DNA extraction. AS revised grammar of English of the manuscript. YW designed the experiment and wrote the paper.

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Correspondence to Yan Wang.

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The authors declare no conflict of interest.

Ethical Approval

This study was conducted following the guideline of Administration of Laboratory Animals published by the State Science and Technology Commission of China (Beijing, China), https://www.lac.zju.edu.cn/cms/26788.

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Yu, C., Zhang, C., Salisu, A. et al. Comparison of the Intestinal Bacteria Between Black Seabass Centropristis striata Reared in Recirculating Aquaculture System and Net Pen. Curr Microbiol 79, 109 (2022). https://doi.org/10.1007/s00284-022-02789-6

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  • DOI: https://doi.org/10.1007/s00284-022-02789-6

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