A Temporally Dynamic Gut Microbiome in Atlantic Salmon During Freshwater Recirculating Aquaculture System (RAS) Production and Post-seawater Transfer

Marlene Lorgen-Ritchie,Samuel A M Martin,Herve Migaud,Lynn Chalmers,Michael Clarkson,John F Taylor

doi:10.3389/fmars.2021.711797

Marlene Lorgen-Ritchie, Samuel A M Martin + Show 4 more

Open Access

https://doi.org/10.3389/fmars.2021.711797

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Abstract

Atlantic salmon aquaculture is undergoing an expansion of land-based recirculating aquaculture systems (RAS), especially for freshwater (FW) stages of production. Juvenile salmon undergo parr-smolt transformation, also known as smoltification and become pre-adapted to tolerate seawater (SW). One aspect requiring study is the development of microbial communities during this time, especially in RAS systems. Here we analyzed temporal changes in microbiome associated with the intestine in Atlantic salmon during smolt production in a commercial RAS production facility and followed the same cohort of fish post-seawater transfer (SWT), using 16S rRNA gene sequencing. Microbial diversity and richness showed an increase over time across FW production, but declined sharply and significantly 1-week post-SWT before re-establishing itself with a completely different community structure after 4 weeks. Core microbial taxa could be assigned to three distinct categories; (1) omnipresent, (2) salinity specific, or (3) transient. By including diet and water samples in the analyses, we classified true core taxa associated with the host, those associated with the diet, and transient cores associated with microbial communities in tank water. The rising trend observed in microbial richness in the water may be a consequence of a temporal increase in organic load while dominance of Vibrionaceae may be attributed to the higher temperatures maintained during RAS production and above average natural water temperatures post-SWT. Functional analysis suggests modulation of metabolic pathways post-SWT, but downstream impacts on fish growth and health in a commercial setting remain to be elucidated. A deeper understanding of the interplay between microbial composition and functionality can play a role in optimizing fish performance in tightly regulated RAS production.

Highlights

The continued growth of the global population coupled with declining wild fish stocks continues to drive expansion of the global aquaculture industry worldwide, with production growing at 7.5% per year since 1970, providing 52% of global fish produced for human consumption in 2018 and generating 250 billion USD first sale value (FAO, 2020)
We investigated the microbiome of Atlantic salmon hindgut reared in a commercial FW recirculating aquaculture systems (RAS) facility, and following transfer to open seawater cages
Temporal trends in alpha diversity in hindgut samples did not mirror those found in water or diet samples, but a rising trend was observed in species richness in water samples from FW2 to FW4

Summary

Introduction

The continued growth of the global population coupled with declining wild fish stocks continues to drive expansion of the global aquaculture industry worldwide, with production growing at 7.5% per year since 1970, providing 52% of global fish produced for human consumption in 2018 and generating 250 billion USD first sale value (FAO, 2020). The parr-smolt transformation (PST) is critical for the long-term health and performance of the stocks, and freshwater environmental conditions (e.g., light, temperature, microbiota, and water quality) and manipulations (e.g., smoltification regimes and vaccination) can impact on the robustness of smolts. Microbial communities in RAS play a vital role in converting waste nutrients from uneaten feed and feces to maintain high water quality, which in turn is critical to fish health (Sullam et al, 2012; Blancheton et al, 2013). Established biofilters in the RAS loop are critical to operational success and contain communities of microbes including nitrifying and denitrifying bacteria which convert potentially toxic by-products of nutrient metabolism such as ammonia into non-toxic forms (Blancheton et al, 2013; Fossmark et al, 2021). Fish mucosal surfaces including skin, gill and gut are always in contact with microbes living in the surrounding water and, in the case of the gut, with feed-associated taxa, presenting opportunities for colonization

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