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In Vitro Profiling of Potential Fish Probiotics, Enterococcus hirae Strains, Isolated from Jade Perch, and Safety Properties Assessed Using Whole Genome Sequencing

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Abstract

The demands of intensified aquaculture production and escalating disease prevalence underscore the need for efficacious probiotic strategies to enhance fish health. This study focused on isolating and characterising potential probiotics from the gut microbiota of the emerging aquaculture species jade perch (Scortum barcoo). Eighty-seven lactic acid bacteria and 149 other bacteria were isolated from the digestive tract of five adult jade perch. The screening revealed that 24 Enterococcus hirae isolates inhibited the freshwater pathogens Aeromonas sobria and Streptococcus iniae. Co-incubating E. hirae with the host gut suspensions demonstrated a two- to five-fold increase in the size of growth inhibition zones compared to the results when using gut suspensions from tilapia (a non-host), indicating host-specificity. Genome analysis of the lead isolate, E. hirae R44, predicted the presence of antimicrobial compounds like enterolysin A, class II lanthipeptide, and terpenes, which underlay its antibacterial attributes. Isolate R44 exhibited desirable probiotic characteristics, including survival at pH values within the range of 3 to 12, bile tolerance, antioxidant activity, ampicillin sensitivity, and absence of transferable antimicrobial resistance genes and virulence factors commonly associated with hospital Enterococcus strains (IS16, hylEfm, and esp). This study offers a foundation for sourcing host-adapted probiotics from underexplored aquaculture species. Characterisation of novel probiotics like E. hirae R44 can expedite the development of disease mitigation strategies to support aquaculture intensification.

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Data Availability

The raw fastq data of E. hirae R44 is available at https://www.ncbi.nlm.nih.gov/sra/PRJNA1013729 with accession number PRJNA1013729.

Abbreviations

RAS:

Recirculating aquaculture system

LAB:

Lactic acid bacteria

BSC:

Biosafety cabinet

PBS:

Phosphate-buffered saline

MRS:

Man, Rogosa, and Sharpe

TSA:

Tryptic soy agar

WCA:

Wilkins-Chalgren anaerobe agar

WCB:

Wilkins-Chalgren anaerobe broth

OD:

Optical density

TSB:

Tryptic soy broth

BHI:

Brain heart infusion

NCBI:

National Centre for Biotechnology Information

BLAST:

Basic Local Alignment Search Tool

CFU:

Colony forming units

BSH:

Bile salt hydrolase

TDC:

Taurodeoxycholate

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

AA%:

Antioxidant activity percentage

WGS:

Whole genome sequencing

bp:

Base pair

QC:

Quality control

AMR:

Antimicrobial resistance

MGEs:

Mobile genetic elements

BGCs:

Biosynthetic gene clusters

VFDB:

Virulence factor database

antiSMASH5:

Antibiotics and Secondary Metabolite Analysis Shell 5.0

BAGEL:

Bacteriocins and RiPP—Ribosomally synthesised and Post-translationally modified Peptides

MIC:

Minimum inhibitory concentration

CLSI:

Clinical and Laboratory Standards Institute

PKSs:

Polyketide synthases

QPS:

Qualified Presumption of Safety

EFSA:

European Food Safety Authority

GRAS:

Generally recognised as safe

EPS:

Exopolysaccharide

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Acknowledgements

The authors gratefully acknowledge Alex Siow of Opal Resources Pte Ltd for providing the jade perch and tilapia used in this study.

Funding

This work was supported by the Singapore Food Agency (SFS_RND_SUFP_001_06), the Ministry of Education (RG79/22 and RT03/21), and Singapore National Biofilm Consortium (SNBC/2021/SF2/P04).

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Authors and Affiliations

  1. NTU Institute for Health Technologies, Interdisciplinary Graduate Programme, Nanyang Technological University, 61 Nanyang Drive, Singapore, 637335, Singapore

    Wenrui Li

  2. School of Materials Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore, 639798, Singapore

    Wenrui Li, Chiun Hao Lim, Zhongtian Zhao & Say Chye Joachim Loo

  3. Singapore Phenome Centre, Lee Kong Chian School of Medicine, Nanyang Technological University, 59 Nanyang Drive, Singapore, 636921, Singapore

    Yulan Wang

  4. Lee Kong Chian School of Medicine, Nanyang Technological University, 59 Nanyang Drive, Singapore, 636921, Singapore

    Yulan Wang & Say Chye Joachim Loo

  5. Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, 60 Nanyang Drive, Singapore, 637551, Singapore

    Patricia Lynne Conway & Say Chye Joachim Loo

  6. Centre for Marine Science Innovation, University of New South Wales, Sydney, NSW, 2052, Australia

    Patricia Lynne Conway

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  1. Wenrui Li
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Contributions

W.R.L., S.C.J.L., Y.L.W., and P.L.C. conceptualised this work. W.R.L. carried out the experiments and gathered and processed the data with C.H.L. and Z.Z.T. W.R.L. drafted the manuscript. S.C.J.L., Y.L.W., and P.L.C. contributed critical feedback to the research, data analysis, and manuscript development. All authors reviewed and approved the final version of the manuscript.

Corresponding author

Correspondence to Say Chye Joachim Loo.

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Li, W., Lim, C.H., Zhao, Z. et al. In Vitro Profiling of Potential Fish Probiotics, Enterococcus hirae Strains, Isolated from Jade Perch, and Safety Properties Assessed Using Whole Genome Sequencing. Probiotics & Antimicro. Prot. (2024). https://doi.org/10.1007/s12602-024-10244-0

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