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

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.

Assessing the Pyloric Caeca and Distal Gut Microbiota Correlation with Flesh Color in Atlantic Salmon (Salmo salar L., 1758)

“…During this time, the fluctuation of water temperature is one of the reasons causing stress in fish [ 5 ] and induces feed reduction or cessation. As a result, water temperature can also affect the fish gut microbiota in Atlantic salmon, as previously demonstrated [ 6 , 7 , 8 ] and confirmed in our recent study [ 9 ], where we showed that changes in the distal gut microbiota profile correlates with flesh color variation across different time points during the relevant period (February–August). Although it is clear that overall temperature fluctuation has an impact on color loss during that period [ 3 ], flesh color variation correlation with the gut microbiota is independent of the change in water temperature [ 9 ], since fish with reduced flesh color have similar microbiota profiles in the distal gut regardless of the time point tested.…”

“…In our previous study [9], a low color index was correlated with Pseudoalteromonadaceae (F), Vibrionaceae (F) and Enterobacteriaceae (F) in the distal gut, which also dominated in the low color group in both gut regions -the distal gut and pyloric caeca -in this study (Figures 5 and 6). Despite the different seasons and environmental conditions between the two studies (the two sampling events took place 2 years apart), Pseudoalteromonadaceae (F), Vibrionaceae (F) and Enterobacteriaceae (F) still persisted in the low color index group, indicating their core position as the symbionts in the altered-symbiosis microbiota composition.…”

“…Therefore, it is possible that Bacillaceae (F) naturally contributes to high-quality flesh. On the other hand, Xanthomonadaceae (F) was the dominant taxon in the carotenoid metabolism pathway in our pervious study [9]. Xanthomonadaceae was firstly found in plants and is able to produce the pigments xanthomonadins [47,48].…”

“…In a previous study, the correlation between the distal gut microbiota and flesh color was demonstrated [9]. This effect was found to occur independently of the water temperature or the season's change.…”

“…The sample details can be found in the Supplementary Material. Digestive tract samples were collected as described in [9]. Briefly, the fish abdomen was incised, and the pyloric caeca and distal part of the intestine ( Figure 2) were aseptically exposed and severed.…”