Abstract

BackgroundThe environment exerts a strong influence on the fish external microbiota, with lower diversity and increased abundances of opportunistic bacterial groups characterizing cultured fish compared to their wild counterparts. Deviation from a healthy external microbiota structure has been associated with increased susceptibility to bacterial pathogens. Treatment of wild-caught broodstock with copper sulfate for the removal of external parasites is a common aquaculture practice. Despite the microbiota’s importance to fish health, the effects of copper sulfate on mucosal bacterial communities and their ability to recover following this chemical treatment have not been examined. The skin microbiota of adult common snook was characterized from wild individuals (Wild), and wild-caught fish maintained in recirculating aquaculture systems (RAS) immediately following a month-long copper sulfate treatment (Captive-1), and then two-weeks (Captive-2) and 2 years (Captive-3) after cessation of copper treatment.ResultsThe skin microbiota of wild fish were characterized by high diversity and taxa including Synechocococcus, SAR11, and a member of the Roseobacter clade. Bacterial diversity decreased in Captive individuals during the 2-year sampling period. Captive fish harbored greater abundances of Firmicutes, which may reflect glycan differences between aquaculture and natural feeds. Bacterial taxa with copper resistance mechanisms and indicative of metal contamination were enriched in Captive-1 and Captive-2 fish. Vibrionaceae were dominant in Captive fish, particularly immediately and 2 weeks following copper treatment. Based on our observations and previous literature, our results suggest putatively beneficial taxa amass over time in captivity. Within 2 years, Captive individuals harbored Bacillus which contains numerous probiotic candidates and the complex carbon degraders of the family Saprospiraceae. Predicted butanoate metabolism exceeded that of Wild fish, and its reported roles in immunity and energy provision suggest a prebiotic effect for fishes.ConclusionsThe mucosal microbiota contains bacterial taxa that may act as bioindicators of environmental pollution. Increases in mutualistic groups indicate a return to a beneficial skin microbiota following copper sulfate treatment. Our data also suggests that vastly different taxa, influenced by environmental conditions, can be associated with adult fish without noticeable health impairment, perhaps due to establishment of various mutualists to maintain fish mucosal health.

Highlights

  • The environment exerts a strong influence on the fish external microbiota, with lower diversity and increased abundances of opportunistic bacterial groups characterizing cultured fish compared to their wild counterparts

  • Culturable bacterial counts Total bacterial counts were highly variable among adult common snook (Table 2)

  • There was no detectable influence of sex on total bacterial counts [F1,24 = 0.907, p = 0.351], and no interaction between sampling period and sex [F2,24 = 1.62, p = 0.219]

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Summary

Introduction

The environment exerts a strong influence on the fish external microbiota, with lower diversity and increased abundances of opportunistic bacterial groups characterizing cultured fish compared to their wild counterparts. Acting as an extension of these defenses, the external mucosa maintains a diverse bacterial assemblage inhabited primarily by commensal microorganisms that help to train the fish immune system and competitively exclude pathogens [2]. Genetic factors, such as mucus composition and immune function, as well as local environmental parameters strongly influence the taxonomic structure of these bacterial communities [2–4]. Adult fish are less susceptible to opportunistic disease than larvae [11], aquaculture practices that decrease bacterial diversity in the fish microbiota relinquish previously inhabited niches within the mucosa that opportunists can colonize, thereby increasing contact rates and potentially harmful interactions between the fish host and aquatic pathogens

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