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Isolation and Characterization of Fish-Gut Bacillus spp. as Source of Natural Antimicrobial Compounds to Fight Aquaculture Bacterial Diseases

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Abstract

Aquaculture is responsible for more than 50% of global seafood consumption. Bacterial diseases are a major constraint to this sector and associated with misuse of antibiotics, pose serious threats to public health. Fish-symbionts, co-inhabitants of fish pathogens, might be a promising source of natural antimicrobial compounds (NACs) alternative to antibiotics, limiting bacterial diseases occurrence in aquafarms. In particular, sporeforming Bacillus spp. are known for their probiotic potential and production of NACs antagonistic of bacterial pathogens and are abundant in aquaculture fish guts. Harnessing the fish-gut microbial community potential, 172 sporeforming strains producing NACs were isolated from economically important aquaculture fish species, namely European seabass, gilthead seabream, and white seabream. We demonstrated that they possess anti-growth, anti-biofilm, or anti-quorum-sensing activities, to control bacterial infections and 52% of these isolates effectively antagonized important fish pathogens, including Aeromonas hydrophila, A. salmonicida, A. bivalvium, A. veronii, Vibrio anguillarum, V. harveyi, V. parahaemolyticus, V. vulnificus, Photobacterium damselae, Tenacibaculum maritimum, Edwardsiela tarda, and Shigella sonnei. By in vitro quantification of sporeformers’ capacity to suppress growth and biofilm formation of fish pathogens, and by assessing their potential to interfere with pathogens communication, we identified three promising candidates to become probiotics or source of bioactive molecules to be used in aquaculture against bacterial aquaculture diseases.

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Data Availability

16S rRNA gene sequences of fish isolates described in this manuscript have been deposited in GenBank with the accession numbers provided in Table 2. Authors confirm that all relevant data are included in the article.

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Acknowledgments

The authors thank F. Tavares (CIBIO-Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Portugal), M. A. Morinigo (Universidad de Málaga, Spain) for the gift of pathogenic bacterial strains, and A. O. Henriques (Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, ITQB-NOVA, Portugal) for the gift of B. subtilis 168.

Funding

RAS is the recipient of a PhD grant (SFRH/BD/131069/2017) from FCT (Foundation for Science and Technology), under the POCH program; PE and CRS have a scientific employment contract supported by national funds through FCT–Portuguese Foundation for Science and Technology. This research was partially supported by the Strategic Funding to UIDB/04423/2020 and UIDP/04423/2020, UIDB/04033/2020 and UIDB/00772/2020 through national funds provided by FCT and European Regional Development Fund (ERDF), in the framework of the program PT2020.

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Authors and Affiliations

  1. Departamento de Biologia, Faculdade de Ciências, Universidade Do Porto, Rua Do Campo Alegre s/n, Ed. FC4, 4169-007, Porto, Portugal

    Rafaela A. Santos, Aires Oliva-Teles, Paula Enes & Cláudia R. Serra

  2. CIIMAR - Centro Interdisciplinar de Investigação Marinha E Ambiental, Terminal de Cruzeiros Do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208, Matosinhos, Portugal

    Rafaela A. Santos, Aires Oliva-Teles, Maria J. Saavedra, Paula Enes & Cláudia R. Serra

  3. CITAB - Centro de Investigação E Tecnologias Agroambientais E Biológicas, Universidade de Trás-Os-Montes E Alto Douro, Quinta de Prados, 5000-801, Vila Real, Portugal

    Rafaela A. Santos & Maria J. Saavedra

  4. CECAV – Centro de Ciência Animal e Veterinária, Universidade de Trás-Os-Montes E Alto Douro, P.O. Box 1013, 5001-801, Vila Real, Portugal

    Rafaela A. Santos & Maria J. Saavedra

  5. Instituto Português Do Mar E da Atmosfera (IPMA), Estação Piloto de Piscicultura de Olhão, Av. 5 de Outubro s/n, 8700-305, Olhão, Portugal

    Pedro Pousão-Ferreira

  6. Epicore Bionetworks Inc., 4 Lina Lane, NJ, 08060, Eastampton, USA

    Russell Jerusik

  7. Departamento de Ciências Veterinárias, ECAV, Universidade de Trás-Os-Montes E Alto Douro, Quinta de Prados, 5000-801, Vila Real, Portugal

    Maria J. Saavedra

Authors
  1. Rafaela A. Santos
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  2. Aires Oliva-Teles
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  3. Pedro Pousão-Ferreira
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  4. Russell Jerusik
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  5. Maria J. Saavedra
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  6. Paula Enes
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  7. Cláudia R. Serra
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Contributions

Conceived and designed the experiments: RAS, AO-T, MJS, PE, CRS. Performed the fish trial: RAS, PP-F, PE. Performed the experiments and analyzed the data: RAS, CRS. Critically evaluated all the data and edited manuscript: RAS, AO-T, RJ, MJS, PE, CRS. Wrote the paper: RAS, CRS. All authors approved the final version of the manuscript.

Corresponding authors

Correspondence to Rafaela A. Santos or Cláudia R. Serra.

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Ethical Approval

Animal experiments were approved by the Animal Welfare Committee of the Interdisciplinary Centre of Marine and Environmental Research (CIIMAR) and carried out in a registered installation (N16091.UDER) and were performed by trained scientists (following FELASA category C recommendations) in full compliance with national rules and following the European Directive 2010/63/EU of the European Parliament and the European Union Council on the protection of animals used for scientific purposes.

Conflict of Interest

RJ is an employee of Epicore Inc., a subsidiary of Archer Daniels Midland, that supported this research by completing a commercial licensing agreement for the potential utilization of the probiotic bacteria FI314, FI330, and FI442 identified in this research, in commercial products for aquaculture. The opinions expressed in the manuscript are those of the authors and do not necessarily reflect company policies. All other authors declare no competing interests.

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Santos, R.A., Oliva-Teles, A., Pousão-Ferreira, P. et al. Isolation and Characterization of Fish-Gut Bacillus spp. as Source of Natural Antimicrobial Compounds to Fight Aquaculture Bacterial Diseases. Mar Biotechnol 23, 276–293 (2021). https://doi.org/10.1007/s10126-021-10022-x

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  • DOI: https://doi.org/10.1007/s10126-021-10022-x

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