Dataset Information

Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures.

ABSTRACT: Host-associated microbiota undergoes a continuous transition, from the birth to adulthood of the host. These developmental stage-related transitions could lead to specific microbial signatures that could impact the host biological processes. In this study, the succession of early-life and intestinal bacterial communities of Atlantic salmon (starting from embryonic stages to 80-week post hatch; wph) was studied using amplicon sequencing of 16S rRNA. Stage-specific bacterial community compositions and the progressive transitions of the communities were evident in both the early life and the intestine. The embryonic communities showed lower richness and diversity (Shannon and PD whole tree) compared to the hatchlings. A marked transition of the intestinal communities also occurred during the development; Proteobacteria were dominant in the early stages (both embryonic and intestinal), though the abundant genera under this phylum were stage-specific. Firmicutes were the most abundant group in the intestine of late freshwater; Weissella being the dominant genus at 20 wph and Anaerofilum at 62 wph. Proteobacteria regained its dominance after the fish entered seawater. Furthermore, LEfSe analysis identified genera under the above - mentioned phyla that are significant features of specific stages. The environmental (water) bacterial community was significantly different from that of the fish, indicating that the host is a determinant of microbial assemblage. Overall the study demonstrated the community dynamics during the development of Atlantic salmon.

SUBMITTER: Lokesh J

PROVIDER: S-EPMC6460355 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures.

Lokesh Jep J Kiron Viswanath V Sipkema Detmer D Fernandes Jorge M O JMO Moum Truls T

MicrobiologyOpen 20180613 4

Host-associated microbiota undergoes a continuous transition, from the birth to adulthood of the host. These developmental stage-related transitions could lead to specific microbial signatures that could impact the host biological processes. In this study, the succession of early-life and intestinal bacterial communities of Atlantic salmon (starting from embryonic stages to 80-week post hatch; wph) was studied using amplicon sequencing of 16S rRNA. Stage-specific bacterial community compositions ...[more]

PMID: 29897674

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Project description:UnlabelledReliance on fishmeal as a primary protein source is among the chief economic and environmental concerns in aquaculture today. Fishmeal-based feeds often require harvest from wild fish stocks, placing pressure on natural ecosystems and causing price instability. Alternative diet formulations without the use of fishmeal provide a potential solution to this challenge. Although the impact of alternative diets on fish performance, intestinal inflammation, palatability, and gut microbiota has been a topic of recent interest, less is known about how alternative feeds impact the aquaculture environment as a whole. The recent focus on recirculating aquaculture systems (RAS) and the closed-containment approach to raising food fish highlights the need to maintain stable environmental and microbiological conditions within a farm environment. Microbial stability in RAS biofilters is particularly important, given its role in nutrient processing and water quality in these closed systems. If and how the impacts of alternative feeds on microbial communities in fish translate into changes to the biofilters are not known. We tested the influence of a fishmeal-free diet on the microbial communities in RAS water, biofilters, and salmon microbiomes using high-throughput 16S rRNA gene V6 hypervariable region amplicon sequencing. We grew Atlantic salmon (Salmo salar) to market size in six replicate RAS tanks, three with traditional fishmeal diets and three with alternative-protein, fishmeal-free diets. We sampled intestines and gills from market-ready adult fish, water, and biofilter medium in each corresponding RAS unit. Our results provide data on how fish diet influences the RAS environment and corroborate previous findings that diet has a clear influence on the microbiome structure of the salmon intestine, particularly within the order Lactobacillales (lactic acid bacteria). We conclude that the strong stability of taxa likely involved in water quality processing regardless of diet (e.g., Nitrospira) may further alleviate concerns regarding the use of alternative feeds in RAS operations.ImportanceThe growth of the aquaculture industry has outpaced terrestrial livestock production and wild-capture fisheries for over 2 decades, currently producing nearly 50% of all seafood consumed globally. As wild-capture fisheries continue to decline, aquaculture's role in food production will grow, and it will produce an estimated 62% of all seafood consumed in 2020. A significant environmental concern of the industry is the reliance on fishmeal as a primary feed ingredient, as its production still requires harvest from wild fisheries. Our study adds to the growing body of literature on the feasibility of alternative, fishmeal-free diets. Specifically, we asked how fishmeal-free diets influence microbial communities in recirculating salmon farms. Unlike previous studies, we extended our investigation beyond the microbiome of the fish itself and asked how alterative diets influence microbial communities in water and critical biofilter habitats. We found no evidence for adverse effects of alternative diets on any microbial habitat within the farm.

Project description:In recent years, a wealth of studies has examined the relationships between a host and its microbiome across diverse taxa. Many studies characterize the host microbiome without considering the ecological processes that underpin microbiome assembly. In this study, the intestinal microbiota of Atlantic salmon, Salmo salar, sampled from farmed and wild environments was first characterized using 16S rRNA gene MiSeq sequencing analysis. We used neutral community models to determine the balance of stochastic and deterministic processes that underpin microbial community assembly and transfer across life cycle stage and between gut compartments. Across gut compartments in farmed fish, neutral models suggest that most microbes are transient with no evidence of adaptation to their environment. In wild fish, we found declining taxonomic and functional microbial community richness as fish mature through different life cycle stages. Alongside neutral community models applied to wild fish, we suggest that declining richness demonstrates an increasing role for the host in filtering microbial communities that is correlated with age. We found a limited subset of gut microflora adapted to the farmed and wild host environment among which Mycoplasma spp. are prominent. Our study reveals the ecological drivers underpinning community assembly in both farmed and wild Atlantic salmon and underlines the importance of understanding the role of stochastic processes, such as random drift and small migration rates in microbial community assembly, before considering any functional role of the gut microbes encountered.IMPORTANCE A growing number of studies have examined variation in the microbiome to determine the role in modulating host health, physiology, and ecology. However, the ecology of host microbial colonization is not fully understood and rarely tested. The continued increase in production of farmed Atlantic salmon, coupled with increased farmed-wild salmon interactions, has accentuated the need to unravel the potential adaptive function of the microbiome and to distinguish resident from transient gut microbes. Between gut compartments in a farmed system, we found a majority of operational taxonomic units (OTUs) that fit the neutral model, with Mycoplasma species among the key exceptions. In wild fish, deterministic processes account for more OTU differences across life stages than those observed across gut compartments. Unlike previous studies, our results make detailed comparisons between fish from wild and farmed environments, while also providing insight into the ecological processes underpinning microbial community assembly in this ecologically and economically important species.

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Dataset Information

Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures.

Publications

Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures.

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