Diet and Host Genetics Drive the Bacterial and Fungal Intestinal Metatranscriptome of Gilthead Sea Bream

Abstract

The gut microbiota is now recognised as a key target for improving aquaculture profit and sustainability, but we still lack insights into the activity of microbes in fish mucosal surfaces. In the present study, a metatranscriptomic approach was used to reveal the expression of gut microbial genes in the farmed gilthead sea bream. Archaeal and viral transcripts were a minority but, interestingly and contrary to rRNA amplicon-based studies, fungal transcripts were as abundant as bacterial ones, and increased in fish fed a plant-enriched diet. This dietary intervention also drove a differential metatranscriptome in fish selected for fast and slow growth. Such differential response reinforced the results of previously inferred metabolic pathways, enlarging, at the same time, the catalogue of microbial functions in the intestine. Accordingly, vitamin and amino acid metabolism, and rhythmic and symbiotic processes were mostly shaped by bacteria, whereas fungi were more specifically configuring the host immune, digestive, or endocrine processes.

Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (Sparus aurata) Production Cycle

“…This finding probably indicates that GS fish do not need to change the composition of their gut microbiota to a high extent to modify their microbial activity to cope with changes in diet composition. It must be noted that the microbial composition of feeds and their potential influence in gut microbiome [ 86 ] was not determined; however, our present results are in accordance with metatranscriptomic analyses that highlighted that the metabolic plasticity of microbiota is higher for the PROGENSA ® offspring in fish families selected for fast growth [ 24 ]. Moreover, this functional feature involved changes in both bacteria and fungi transcripts, which highly enlarges the catalogue of microbial functions in the fish intestine.…”

“…Similarly, the nutritionally regulated genes decreased from 459 DE transcripts (415 UD) in GS to 9 DE transcripts (9 UD) in REF fish when comparisons were made for a given lineage between CTRL- and FUTURE-fed fish. This host transcriptional regulation is, thereby, similar to that reported for the genetically and nutritionally regulated composition of gut microbiota in this and previous metagenomics [ 23 ] and metatranscriptomic [ 24 ] studies after selective breeding for fast-growth in the PROGENSA ® program. Therefore, it appears conclusive that both the gut microbiota and host-transcriptomic patterns are structurally stable, but at the same time more plastic is present at the functional level in fish with an improved growth potentiality.…”

“…The interaction between diet and genetics remains relatively poorly studied in fish [ 23 , 75 , 80 ]. However, it is generally accepted that the high replacement of dietary marine feedstuffs (FM/FO) has very often had an impact on growth performance [ 81 , 82 , 83 , 84 ] and intestinal health [ 23 , 85 ] due, at least in part, to changes in gut microbiota [ 22 , 24 ]. Moreover, there is now evidence that the offspring of F1/F2 crosses for fast growing families in the PROGENSA ® selection program disclosed a more resilient and plastic microbiota in fish grow out in the Mediterranean aquaculture infrastructure of IATS-CSIC [ 23 ].…”

“…The same cannot be said for host genetics, whose influence on the composition and activity of gut microbiota remains less investigated. However, recent studies in gilthead sea bream pointed out that intensive selection for fast-growth co-selects for a plastic gut microbiota with a wider metabolic response to cope with changes in diet composition [ 23 , 24 ]. Links between gut microbiota and the host-transcriptome have also been established in gilthead sea bream, using targeted [ 17 , 18 , 22 ] or massive gene expression [ 25 ] approaches.…”

Use of male-to-female sex reversal as a welfare scoring system in the protandrous farmed gilthead sea bream (Sparus aurata)

“…The rationale for this procedure is that the complex balance of environmental variables that regulate animal welfare conditions can also affect sex change in sequential hermaphrodites. To pursue this issue, sex reversal was monitored in fish families with different nutritional backgrounds and different heritable growth within the PROGENSA ® selection program ( 42 ), which co-selected among other traits with changes in gut microbiota composition and metabolic plasticity ( 5 , 43 ), as well as swimming performance and aerobic scope ( 44 , 45 ).…”