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Atlantic Salmon (Salmo salar L., 1758) Gut Microbiota Profile Correlates with Flesh Pigmentation: Cause or Effect?

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Abstract

In Tasmania (Australia), during the marine phase, it has been observed that flesh pigmentation significantly drops in summer, possibly due to high water temperatures (> 20 °C). Although this deleterious effect of summer temperatures has been ascertained, there is a lack of knowledge of the actual mechanisms behind the impaired uptake and/or loss of pigments in Atlantic salmon in a challenging environment. Since the microbial community in the fish intestine significantly changes in relation to the variations of water temperature, this study was conducted to assess how the gut microbiota profile also correlates with the flesh color during temperature fluctuation. We sampled 68 fish at three time points covering the end of summer to winter at a marine farm in Tasmania, Australia. Flesh color was examined in two ways: the average color throughout and the evenness of the color between different areas of the fillet. Using 16S rRNA sequencing of the v3–v4 region, we determined that water temperature corresponded to changes in the gut microbiome both with alpha diversity (Kruskal-Wallis tests P = 0.05) and beta diversity indices (PERMANOVA P = 0.001). Also, there was a significant correlation between the microbiota and the color of the fillet (PERMANOVA P = 0.016). There was a high abundance of Pseudoalteromonadaceae, Enterobacteriaceae, Microbacteriaceae, and Vibrionaceae in the pale individuals. Conversely, carotenoid-synthesizing bacteria families (Bacillaceae, Mycoplasmataceae, Pseudomonas, Phyllobacteriaceae, and Comamonadaceae) were found in higher abundance in individuals with darker flesh color.

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Availability of Data and Material

The metadata file, rarefied, and unrarefied OTU tables, and sequences files used in this study are undergoing the process of deposition in the European Bioinformatics Institute (EBI) repository. The metadata file can be found in Supplemental Material S1. The full records of core diversities and differentiation analysis are included as Supplemental Material S2 and S3, respectively, which are also undergoing the process of deposition in EBI as qzv and qza file type.

Abbreviations

Ax:

astaxanthin

(C):

class

Cx:

canthaxanthin

(F):

family

(G):

genus

KEGG:

Kyoto Encyclopedia of Genes and Genomes

KO:

KEGG Orthology

LDA:

Linear Discriminant Analysis

LEfSE:

linear discriminant analysis effect size

(O):

order

OTU:

Operational Taxonomic Unit

(P):

phylum

PICRUSt:

Phylogenetic Investigation of Communities by Reconstruction of Unobserved States

QIIME:

Quantitative Insights into Microbial Ecology

(S):

species

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Acknowledgments

The authors would like to acknowledge Petuna Aquaculture, Stuart Atherton, Tom Fox-Smith, and Ryan Wilkinson for their contribution to this project.

Funding

The research was funded by the Fisheries Research and Development Corporation FRDC (project code: FRDC 2014-248) through a collaboration between Petuna Aquaculture and the University of the Sunshine Coast. CDHN was supported by an International postgraduate award from the University of the Sunshine Coast.

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Authors and Affiliations

  1. GeneCology Research Centre, University of the Sunshine Coast, 4 Locked Bag, Maroochydore, Queensland, 4558, Australia

    Chan D. H. Nguyen, Gianluca Amoroso, Tomer Ventura & Abigail Elizur

  2. Petuna Aquaculture, 134 Tarleton Street, East Devonport, Tasmania, 7310, Australia

    Gianluca Amoroso

  3. Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, 92037, USA

    Jeremiah J. Minich

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  1. Chan D. H. Nguyen
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Contributions

Conceived and designed the experiments: CDHN, GA, TV, and AE. Collected samples: GA. Performed the experiments: CDHN. Analyzed the data: CDHN and JM. Wrote the paper: CDHN. All authors contributed to the paper drafts and accepted the manuscript.

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Correspondence to Abigail Elizur.

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All procedures were carried out with the approval of the University of the Sunshine Coast Animal Ethics Committee (AN/E/16/12).

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Nguyen, C.D.H., Amoroso, G., Ventura, T. et al. Atlantic Salmon (Salmo salar L., 1758) Gut Microbiota Profile Correlates with Flesh Pigmentation: Cause or Effect?. Mar Biotechnol 22, 786–804 (2020). https://doi.org/10.1007/s10126-019-09939-1

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