1887

Abstract

Microbiome components and bacterial isolates related to healthy and epitheliocystis states in aquaculture cycles of cobia fish were studied. We detected well-defined 16S rRNA amplicon gene sequence variants showing differential abundance in healthy or diseased cycles. Isolation trials were performed, and experimental tests were used to determine probiotic potential of the bacterial strains obtained from water, tissues or live food used in this aquaculture model. The taxonomic affiliation of these strains was cross-compared against microbiome components, finding that some of them had close or identical affiliation to the abundant types found in healthy cycles. Strains belonging to the groups already identified as predominant by culture-independent means were screened as potential probiotics based on desirable activities such as antagonism and antibiosis against marine pathogenic bacteria, quorum quenching, bile acid resistance, antibiotic sensitivity and enzymatic activities for improved nutrient digestion. We have also found that in the tracking of microbiome composition across different developmental stages of cobia, healthy cycles exhibited a consistent high relative abundance of a sp., while in the diseased cycle the emergence of a sp. was observed. Our study suggests that epithelocystis in cobia is associated with a displacement of a symbiotic microbiome community linked to the increase frequency of species.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000405
2022-08-10
2024-07-24
Loading full text...

Full text loading...

/deliver/fulltext/acmi/4/8/acmi000405.html?itemId=/content/journal/acmi/10.1099/acmi.0.000405&mimeType=html&fmt=ahah

References

  1. Benetti DD, Orhun MR, Sardenberg B, O’Hanlon B, Welch A et al. Advances in hatchery and grow-out technology of cobia Rachycentron canadum (Linnaeus). Aquaculture Res 2008; 39:701–711 [View Article]
    [Google Scholar]
  2. Rameshkumar P, Abdul Nizar M, Jayakumar R, Tamilmani G, Sakthivel M et al. Development of a multivalent vibriosis vaccine and its application in sea cage farming of cobia. Marine Fisheries Information Service, Technical and Extension Series 2020; 246:29–33
    [Google Scholar]
  3. Lafferty KD, Harvell CD, Conrad JM, Friedman CS, Kent ML et al. Infectious diseases affect marine fisheries and aquaculture economics. Ann Rev Mar Sci 2015; 7:471–496 [View Article] [PubMed]
    [Google Scholar]
  4. Mendoza M, Güiza L, Martinez X, Caraballo X, Rojas J et al. A novel agent (Endozoicomonas elysicola) responsible for epitheliocystis in cobia Rachycentrum canadum larvae. Dis Aquat Organ 2013; 106:31–37 [View Article] [PubMed]
    [Google Scholar]
  5. Bayer T, Arif C, Ferrier-Pagès C, Zoccola D, Aranda M et al. Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar Ecol Prog Ser 2013; 479:75–84 [View Article]
    [Google Scholar]
  6. Sanchez LM, Wong WR, Riener RM, Schulze CJ, Linington RG et al. Examining the fish microbiome: vertebrate-derived bacteria as an environmental niche for the discovery of unique marine natural products. PLoS One 2012; 7:e35398 [View Article] [PubMed]
    [Google Scholar]
  7. Legrand TPRA, Catalano SR, Wos-Oxley ML, Stephens F, Landos M et al. The inner workings of the outer surface: skin and gill microbiota as indicators of changing gut health in Yellowtail Kingfish. Front Microbiol 2017; 8:2664 [View Article] [PubMed]
    [Google Scholar]
  8. Leonard AB, Carlson JM, Bishoff DE et al. The skin microbiome of Gambusia affinis is defined and selective. Adv Microbiol 2014 [View Article]
    [Google Scholar]
  9. Yilmaz S, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E et al. Probiotics, prebiotics, and synbiotics used to control vibriosis in fish: a review. Aquaculture 2022; 547:737514 [View Article]
    [Google Scholar]
  10. Edwards P. Aquaculture environment interactions: past, present and likely future trends. Aquaculture 2015; 447:2–14 [View Article]
    [Google Scholar]
  11. Geng X, Dong XH, Tan BP, Yang QH, Chi SY et al. Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish Shellfish Immunol 2011; 31:400–406 [View Article] [PubMed]
    [Google Scholar]
  12. Garrido Pereira MA, Schwarz M, Delbos B, Rodrigues RV, Romano L et al. Probiotic effects on cobia Rachycentron canadum larvae reared in a recirculating aquaculture system. lajar 2014; 42:1169–1174 [View Article]
    [Google Scholar]
  13. Amenyogbe E, Chen G, Wang Z, Huang J, Huang B et al. The exploitation of probiotics, prebiotics and synbiotics in aquaculture: present study, limitations and future directions.: a review. Aquacult Int 2020; 28:1017–1041 [View Article]
    [Google Scholar]
  14. Cawthorn DM, Steinman HA, Witthuhn RC. Comparative study of different methods for the extraction of DNA from fish species commercially available in South Africa. Food Control 2011; 22:231–244 [View Article]
    [Google Scholar]
  15. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 2000; 66:5488–5491 [View Article] [PubMed]
    [Google Scholar]
  16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6:1621–1624 [View Article] [PubMed]
    [Google Scholar]
  17. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4516–4522 [View Article] [PubMed]
    [Google Scholar]
  18. Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG et al. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics 2011; Chapter 10:Unit [View Article] [PubMed]
    [Google Scholar]
  19. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8:e61217 [View Article] [PubMed]
    [Google Scholar]
  20. Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 2010; 4:17–27 [View Article] [PubMed]
    [Google Scholar]
  21. Barberán A, Bates ST, Casamayor EO, Fierer N et al. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 2012; 6:343–351 [View Article] [PubMed]
    [Google Scholar]
  22. Villamil L, Figueras A, Planas M, Novoa B et al. Pediococcus acidilactici in the culture of turbot (Psetta maxima) larvae: Administration pathways. Aquaculture 2010; 307:83–88 [View Article]
    [Google Scholar]
  23. Murillo I, Villamil L. Bacillus cereus and Bacillus subtilis used as probiotics in rotifer (Brachionus plicatilis) cultures. J Aquac Res Development 2011; s1:1–5 [View Article]
    [Google Scholar]
  24. Villamil L, Reyes C, Martínez-Silva MA. In vivo and in vitro assessment of Lactobacillus acidophilus as probiotic for tilapia (Oreochromis niloticus, Perciformes:Cichlidae) culture improvement. Aquacul Res 2014
    [Google Scholar]
  25. Erkkilä S, Petäjä E. Screening of commercial meat starter cultures at low pH and in the presence of bile salts for potential probiotic use. Meat Sci 2000; 55:297–300 [View Article]
    [Google Scholar]
  26. Chakravorty S, Helb D, Burday M, Connell N, Alland D et al. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods 2007; 69:330–339 [View Article] [PubMed]
    [Google Scholar]
  27. Mclean E, Salze G, Craig SR. Parasites, disease and deformities of cobia. Ribarstvo 2008; 66:1–16
    [Google Scholar]
  28. Risøen PA, Rønning P, Hegna IK, Kolstø A-B et al. Characterization of a broad range antimicrobial substance from Bacillus cereus. J Appl Microbiol 2004; 96:648–655 [View Article] [PubMed]
    [Google Scholar]
  29. Ramirez RF, Dixon BA. Enzyme production by obligate intestinal anaerobic bacteria isolated from oscars (Astronotus ocellatus) angelfish (Pterophyllum scalare) and southern flounder (Paralichthys lethostigma). Aquaculture 2003; 227:417–426
    [Google Scholar]
  30. Nithya C, Begum MF, Pandian SK. Marine bacterial isolates inhibit biofilm formation and disrupt mature biofilms of Pseudomonas aeruginosa PAO1. Appl Microbiol Biotechnol 2010; 88:341–358 [View Article] [PubMed]
    [Google Scholar]
  31. Ahmed I, Yokota A, Fujiwara T. A novel highly boron tolerant bacterium, Bacillus boroniphilus sp. nov., isolated from soil, that requires boron for its growth. Extremophiles 2007; 11:217–224 [View Article] [PubMed]
    [Google Scholar]
  32. Han Y, Li X, Qi Z, Zhang X-H, Bossier P et al. Detection of different quorum-sensing signal molecules in a virulent Edwardsiella tarda strain LTB-4. J Appl Microbiol 2010; 108:139–147 [View Article] [PubMed]
    [Google Scholar]
  33. Le MH, Dinh KV, Nguyen MV, Rønnestad I. Combined effects of a simulated marine heatwave and an algal toxin on a tropical marine aquaculture fish cobia (Rachycentron canadum). Aquac Res 2020; 51:2535–2544 [View Article]
    [Google Scholar]
  34. Wu YL, Lee MA, Chen LC, Chan JW, Lan KW. Evaluating a suitable aquaculture site selection model for cobia (Rachycentron canadum) during extreme events in the inner Bay of the Penghu Islands, Taiwan. Remote Sens 2020; 12:2689 [View Article]
    [Google Scholar]
  35. Pawlikowska-Warych M, Deptuła W. Characteristics of chlamydia-like organisms pathogenic to fish. J Appl Genet 2016; 57:135–141 [View Article] [PubMed]
    [Google Scholar]
  36. Turnbull JF, Richards RH, Tatner MF. Evidence that superficial branchial colonies on the gills of Salmo salar L. are not Aeromonas salmonicida. J Fish Diseases 1989; 12:449–458 [View Article]
    [Google Scholar]
  37. Phillips ACN, Suepaul R, Soto E. Ocular localization of mycobacterial lesions in tank-reared juvenile cobia, Rachycentron canadum. J Fish Dis 2017; 40:1799–1804 [View Article] [PubMed]
    [Google Scholar]
  38. Liu PC, Lin JIY, Lee KK. Virulence of Photobacterium damselae subsp. piscicida in cultured cobia Rachycentron canadum. J Basic Microbiol 2003; 43:499–507 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000405
Loading
/content/journal/acmi/10.1099/acmi.0.000405
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error