Expanding the use of circulating microbiome in fish: contrast between the gut and blood microbiome of Sebastes fasciatus

Abstract

The study of microbiomes in fish populations offers vital insights for ecological and fisheries management, particularly in responses to environmental changes. Although traditional studies have concentrated on the gut microbiome, the emerging concept of a circulating blood microbiome suggests it may act as an early indicator of dysbiosis and various health conditions by reflecting transient bacterial DNA presence. In this study, we examined the gut and blood microbiomes of Sebastes fasciatus (Storer, 1854), a species of redfish of significant economic and ecological importance in the Gulf of St. Lawrence, to obtain critical information for health monitoring, pathogen detection, and ecological management in fisheries. Our results revealed that the gut and blood microbiomes of S. fasciatus have distinct bacterial DNA signatures, with significant differences in microbial diversity. Notably, although both microbiomes exhibited similar dominant genera, specific amplicon sequence variants varied significantly. Through a controlled experimental design, we found that the dietary impacts on microbiome composition were statistically significant yet minimal, suggesting that environmental factors play a more substantial role in shaping microbial communities. Finally, we report the presence of potential pathogens and opportunistic bacteria found exclusively in the blood microbiome. Our results highlight the blood microbiome's value as a sensitive health and environmental stress indicator, essential for sustainable fish population management. Integrating microbiome indicators can improve fisheries management and ecosystem sustainability, offering a model applicable to various marine species and environments.

Keywords: 16S rRNA gene; Gulf of St. Lawrence; Sebastes; blood; diet; fish; gut; microbiome.

Graphical Abstract

Figure 1

Experimental design and sampling strategy for the dietary study on Sebastes fasciatus. Figure illustrating the layout and protocol of a six-month dietary intervention study involving 225 S. fasciatus, distributed among 15 tanks at a density of 15 fish per tank. The study included five distinct dietary regimens, each replicated across three tanks. At the conclusion of the experiment, a subset of 90 fish (six from each tank) was selected for detailed analyses. From these selected fish, 88 gut samples were preserved by freezing at −20°C for subsequent analysis, and blood samples were collected from 89 fish and stored on FTA cards for DNA analysis. The figure details the tank distribution, dietary assignment, and sampling regimen used in the study.

Figure 2

Relative abundance of the main taxa in the blood and gut microbiome. (A) Individual relative abundance of the main phylum of the Redfish’s microbiome, prevalence = 50%, detection threshold = 1%, n (gut) = 86 and n (blood) = 89. (B) Mean by tank of the relative abundance of the main genera of the Redfish’s microbiome, prevalence = 30%, detection threshold = 1%, n (gut) = 86 and n (blood) = 89.

Figure 3

Differences between the blood and gut microbiomes. (A) Unique and shared genera. (B) PCoA plot of the microbial communities found in two distinct biological niches, ellipses represent an estimation of a t-distribution around the centroids, n (gut) = 86 and n (blood) = 89. (C) A comparison of diversity indices and relative abundance metrics of microbial communities between the two biological niches. Prevalence = 50%; detection threshold = 1%; n (gut) = 86 and n (blood) = 89. 9; ^*P < .05, ^**P < .01, ^***P < .001.

Figure 4

Significant differences in ASVs observed between the niches. (A) Differential abundance of ASVs between blood and gut niches as indicated by ANCOM-BC LogFoldChange values. (B) Bubbleplot of the ASV with a significant differential abundance between niches. Each point represents an ASV. The larger a point appears on the graph, the greater the disparity in ASV abundance between the niches. Gut (n = 86); Blood (n = 89).

Figure 5

PCoA of microbiome diversity in different treatment groups. The left panel shows a PCoA plot that displays the microbial diversity in the gut across various treatment groups, visualized along two principal coordinate axes explaining 10.5% and 8.7% of the variance, respectively. The right panel illustrates the microbial diversity in the circulating microbiome, with axes explaining 15.1% and 9.0% of the variance, respectively. Ellipses represent an estimation of a t-distribution around the centroids of each group. Statistical significance between groups is indicated, with PERMANOVA results showing variations in microbial composition between treatments.