Diet, Immunity, and Microbiota Interactions: An Integrative Analysis of the Intestine Transcriptional Response and Microbiota Modulation in Gilthead Seabream (Sparus aurata) Fed an Essential Oils-Based Functional Diet

Abstract

Essential oils (EOs) are promising alternatives to chemotherapeutics in animal production due to their immunostimulant, antimicrobial, and antioxidant properties, without associated environmental or hazardous side effects. In the present study, the modulation of the transcriptional immune response (microarray analysis) and microbiota [16S Ribosomal RNA (rRNA) sequencing] in the intestine of the euryhaline fish gilthead seabream (Sparus aurata) fed a dietary supplementation of garlic, carvacrol, and thymol EOs was evaluated. The transcriptomic functional analysis showed the regulation of genes related to processes of proteolysis and inflammatory modulation, immunity, transport and secretion, response to cyclic compounds, symbiosis, and RNA metabolism in fish fed the EOs-supplemented diet. Particularly, the activation of leukocytes, such as acidophilic granulocytes, was suggested to be the primary actors of the innate immune response promoted by the tested functional feed additive in the gut. Fish growth performance and gut microbiota alpha diversity indices were not affected, while dietary EOs promoted alterations in bacterial abundances in terms of phylum, class, and genus. Subtle, but significant alterations in microbiota composition, such as the decrease in Bacteroidia and Clostridia classes, were suggested to participate in the modulation of the intestine transcriptional immune profile observed in fish fed the EOs diet. Moreover, regarding microbiota functionality, increased bacterial sequences associated with glutathione and lipid metabolisms, among others, detected in fish fed the EOs supported the metabolic alterations suggested to potentially affect the observed immune-related transcriptional response. The overall results indicated that the tested dietary EOs may promote intestinal local immunity through the impact of the EOs on the host-microbial co-metabolism and consequent regulation of significant biological processes, evidencing the crosstalk between gut and microbiota in the inflammatory regulation upon administration of immunostimulant feed additives.

Phytogenic Bioactive Compounds Shape Fish Mucosal Immunity

“…In addition, the above-mentioned study revealed that the tested phytogenic compounds promoted the presence of sialic-acids containing glycoproteins in both epithelial and mucous cells, which globally resulted in a decrease in the intensity of gills' infestation by the monogenean ectoparasite Sparicotyle chrysophrii in gilthead seabream (15). Both, referred phytogenics combinations were observed to positively affect the gut health status of those fish species by improving the protective intestine mucus coverage post-challenge ( 13), regulating the intestine immune transcription (12) and modulating their intestinal microbiota (12,105).…”

“…Phytogenic administration has the potential to regulate the mucosal barrier function by means of several molecular mechanisms, in which the phytogenic bioactive compounds interact with cellular transcription factors and metabolic cascades. Therefore, the modulation of the expression of genes coding for immune relevant molecules alter the mucosal protective characteristics and their immunological status (12)(13)(14)(15)(16). Besides, the immune system influences the regulation and composition of the microbiota and vice versa, an interaction that plays a determinant role in the maintenance of the mucosal integrity and functionality (17,18).…”

The Applicability of Essential Oils in Different Stages of Production of Animal-Based Foods

“…Essential oils are added to feed and water as taste enhancers, and they are also administered to boost immunity and improve the performance of poultry [16,21]. − exact mechanisms are still elusive [63] Since in vitro studies (cited above) have confirmed the antimicrobial efficacy of EOs, they can be used as natural growth promoters in livestock nutrition, in particular in poultry and pig farming [6]. Essential oils enhance the flavor and palatability of feeds, in particular those deficient in these attributes, which improves feed intake.…”

“…The results of different studies analyzing the effects of dietary supplementation with EOs or their active ingredients on the health status and performance of animals are presented by many authors [47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63].…”

“…Porcine diets supplemented with EOs enhance the immune response of piglets at weaning [6,32]. In fish diets, EOs may promote local intestinal immunity through the impact on the host-microbial co-metabolism [63]. The antimicrobial activities of EOs can also affect ruminal fermentation [50].…”