Alternative Protein Sources in the Diet Modulate Microbiota and Functionality in the Distal Intestine of Atlantic Salmon (Salmo salar)

Abstract

The present study aimed to investigate whether alternative dietary protein sources modulate the microbial communities in the distal intestine (DI) of Atlantic salmon, and whether alterations in microbiota profiles are reflected in modifications in host intestinal function and health status. A 48-day feeding trial was conducted, in which groups of fish received one of five diets: a reference diet in which fishmeal (diet FM) was the only protein source and four experimental diets with commercially relevant compositions containing alternative ingredients as partial replacements of fishmeal, i.e., poultry meal (diet PM), a mix of soybean meal and wheat gluten (diet SBMWG), a mix of soy protein concentrate and poultry meal (diet SPCPM), and guar meal and wheat gluten (diet GMWG). Samples were taken of DI digesta and mucosa for microbial profiling using high-throughput sequencing and from DI whole tissue for immunohistochemistry and expression profiling of marker genes for gut health. Regardless of diet, there were significant differences between the microbial populations in the digesta and the mucosa in the salmon DI. Microbial richness was higher in the digesta than the mucosa. The digesta-associated bacterial communities were more affected by the diet than the mucosa-associated microbiota. Interestingly, both legume-based diets (SBMWG and GMWG) presented high relative abundance of lactic acid bacteria in addition to alteration in the expression of a salmon gene related to cell proliferation (pcna). It was, however, not possible to ascertain the cause-effect relationship between changes in bacterial communities and the host's intestinal responses to the diets.IMPORTANCE The intestine of cultivated Atlantic salmon shows symptoms of compromised function, which are most likely caused by imbalances related to the use of new feed ingredients. Intestinal microbiota profiling may become in the future a valuable endpoint measurement in order to assess fish intestinal health status and effects of diet. The present study aimed to gain information about whether alternative dietary protein sources modulate the microbial communities in the Atlantic salmon intestine and whether alterations in microbiota profiles are reflected in alterations in host intestinal function and health status. We demonstrate here that there are substantial differences between the intestinal digesta and mucosa in the presence and abundance of bacteria. The digesta-associated microbiota showed clear dependence on the diet composition, whereas mucosa-associated microbiota appeared to be less affected by diet composition. Most important, the study identified bacterial groups associated with diet-induced gut dysfunction that may be utilized as microbial markers of gut health status in fish.

Dietary live yeast and increased water temperature influence the gut microbiota of rainbow trout

“…In addition, the results show that bacterial diversity in the gut content was higher than that in the gut mucosa of rainbow trout, which has been shown previously in Atlantic salmon (Gajardo et al . , ). In contrast, high‐throughput sequencing studies on rainbow trout and Asian seabass have shown no differences in bacterial diversity between gut content and mucosa (Lyons et al .…”

“…) and Atlantic salmon (Gajardo et al . ) fed diets with higher inclusion levels of FM. Similarly, the present study found higher abundances of Photobacterium in the FM diets and in the gut content of fish fed FM, at least in cold water (Figs and ).…”

Current Advances in Functional Genomics in Aquaculture

“…Moreover, the PI showed presence of Spirochaetes that were not found in the MI showing that metagenomics can be used to identify microbial communities that inhabit diferent segments of the gut. In another study, Gajardo et al [11] identiied bacterial groups associated with diet-induced gut dysfunction that could serve as biological markers of the gut health status in Atlantic salmon. Mouchet et al [73] compared the gut microbiota of 15 ish species from the Atlantic Ocean near Brazil and showed that the microbiota genetic diversity was highly inluenced by the ish species, geographical location and diet.…”

“…In terms of assembly, both whole genome shotgun and marker gene guided sequencing have been used on diferent aquatic organisms. The commonly used marker gene in metagenomics analyses is the 16S ribosomal RNA (16S rRNA), which has been widely used to characterize the microbiota of diferent aquatic organisms including rainbow trout [88,89], Atlantic salmon [11,12], turbot (Scophthalmus maximus) [90], lamprey (Lampetra morii) [91] and Baleen whale [92]. Whole genome shotgun sequencing has also been widely used in the study of environmental microbial communities and pathogens infecting diferent aquatic organisms.…”

“…These omics technologies have not only accelerated whole genome sequencing projects of diferent aquatic organisms [7,8], but they also have the capacity to unravel the sequences of entire genomes without prior knowledge of the genes to be sequenced thereby enhancing the discovery and annotation of novel genes in non-model species. And as shown from recent studies, their applications in aquaculture have accelerated our ability to identify emerging pathogens [9], monitor the microbiomes of diferent aquatic environments [10], develop nutritional diets with less side efects [11,12] and understand the cellular networks that regulate diferent biological processes in aquatic organisms [13][14][15]. It is evident from studies carried out this far that an integrated use of different omics technologies is bound to improve our production systems in aquaculture [10,12,[16][17][18].…”