Disruption of gut integrity and permeability contributes to enteritis in a fish-parasite model: a story told from serum metabolomics

Sitjà‐Bobadilla, Ariadna; Gil-Solsona, Rubén; Estensoro, Itziar; Piazzon, M. Carla; Martos-Sitcha, Juan Antonio; Picard‐Sánchez, Amparo; Fuentes, Juan; Sancho, Juan V.; Calduch-Giner, Josep Àlvar; Hernández, Félix

doi:10.1186/s13071-019-3746-7

Cited by 27 publications

(14 citation statements)

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“…However, this is not universal, as growth selection was found to be positively correlated with disease susceptibility in other fish species when facing bacterial or viral challenges [ 87 , 88 ]. The parasite used in this study, E. leei , invades the paracellular space between the enterocytes, where it lives and divides [ 89 ], causing severe enteritis linked to the disruption of tight junctions and loss of intestinal barrier function [ 90 ]. Remarkably, even though all groups got infected, the fast-growth families showed lower parasite abundance, intensity of infection, and lower disease signs.…”

Section: Discussionmentioning

confidence: 99%

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

et al. 2020

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Background The key effects of intestinal microbiota in animal health have led to an increasing interest in manipulating these bacterial populations to improve animal welfare. The aquaculture sector is no exception and in the last years, many studies have described these populations in different fish species. However, this is not an easy task, as intestinal microbiota is composed of very dynamic populations that are influenced by different factors, such as diet, environment, host age, and genetics. In the current study, we aimed to determine whether the genetic background of gilthead sea bream (Sparus aurata) influences the intestinal microbial composition, how these bacterial populations are modulated by dietary changes, and the effect of selection by growth on intestinal disease resistance. To that aim, three different groups of five families of gilthead sea bream that were selected during two generations for fast, intermediate, or slow growth (F3 generation) were kept together in the same open-flow tanks and fed a control or a well-balanced plant-based diet during 9 months. Six animals per family and dietary treatment were sacrificed and the adherent bacteria from the anterior intestinal portion were sequenced. In parallel, fish of the fast- and slow-growth groups were infected with the intestinal parasite Enteromyxum leei and the disease signs, prevalence, intensity, and parasite abundance were evaluated. Results No differences were detected in alpha diversity indexes among families, and the core bacterial architecture was the prototypical composition of gilthead sea bream intestinal microbiota, indicating no dysbiosis in any of the groups. The plant-based diet significantly changed the microbiota in the intermediate- and slow-growth families, with a much lower effect on the fast-growth group. Interestingly, the smaller changes detected in the fast-growth families potentially accounted for more changes at the metabolic level when compared with the other families. Upon parasitic infection, the fast-growth group showed significantly lower disease signs and parasite intensity and abundance than the slow-growth animals. Conclusions These results show a clear genome-metagenome interaction indicating that the fast-growth families harbor a microbiota that is more flexible upon dietary changes. These animals also showed a better ability to cope with intestinal infections.

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Section: Discussionmentioning

confidence: 99%

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

et al. 2020

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“…However, this is not universal, as growth selection was found to be positively correlated with disease susceptibility in other sh species when facing bacterial or viral challenges [87,88]. The parasite used in this study, E. leei, invades the paracellular space between the enterocytes, where it lives and divides [89], causing severe enteritis linked to the disruption of tight junctions and loss of intestinal barrier function [90]. Remarkably, even though all groups got infected, the fast-growth families showed lower parasite abundance, intensity of infection, and lower disease signs.…”

Section: Discussionmentioning

confidence: 94%

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Piazzon

Naya-Català

Perera

et al. 2020

Preprint

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Background: The key effects of intestinal microbiota in animal health has led to an increasing interest in manipulating these bacterial populations to improve animal welfare. The aquaculture sector is no exception and in the last years many studies have described these populations in different fish species. However, this is not an easy task, as intestinal microbiota is composed of very dynamic populations that are influenced by different factors, such as diet, environment, host age and genetics. In the current study, we aimed to determine whether the genetic background of gilthead sea bream (Sparus aurata) influences the intestinal microbial composition, how these bacterial populations are modulated by dietary changes, and the effect of selection by growth on intestinal disease resistance. To that aim, three different groups of five families of gilthead sea bream that were selected during two generations for fast, intermediate or slow growth (F3 generation) were kept together in the same open-flow tanks and fed a control or a well-balanced plant-based diet during nine months. Six animals per family and dietary treatment were sacrificed and the adherent bacteria from the anterior intestinal portion were sequenced. In parallel, fish of the fast- and slow-growth groups were infected with the intestinal parasite Enteromyxum leei and the disease signs, prevalence, intensity and parasite abundance were evaluated. Results: No differences were detected in alpha diversity indexes among families, and the core bacterial architecture was the prototypical composition of gilthead sea bream intestinal microbiota, indicating no dysbiosis in any of the groups. The plant-based diet significantly changed the microbiota in the intermediate- and slow-growth families, with a much lower effect on the fast-growth group. Interestingly, the smaller changes detected in the fast-growth families potentially accounted for more changes at the metabolic level when compared to the other families. Upon parasitic infection, the fast-growth group showed significantly lower disease signs and parasite intensity and abundance than the slow-growth animals. Conclusions: These results show a clear genome-metagenome interaction indicating that the fast-growth families harbor a microbiota that is more flexible upon dietary changes. These animals also showed a better ability to cope with intestinal infections.

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“…IgM + cells massively proliferate in the submucosa and within the epithelium (27), whereas Zap70 + T cells aggregate mainly at the base of the epithelium (28). This inflammatory response, together with enterocyte apoptosis and necrosis, hamper intestinal barrier integrity producing nutrient malabsorption and osmotic intestinal failure (31). As expected, these signs were also observed in the current experiment, where challenged fish showed an inflammatory response in the submucosa with abundant Zap70 + T cells at the base of the epithelium and infiltrated in it.…”

Section: Discussionmentioning

confidence: 99%

“…E. leei induces IgM and IgT gene expression both at local (intestine) and systemic levels (head kidney), with a potent local effect. This increased gene expression has been correlated with increased serum levels of parasite-specific IgM (29,31). Regretfully, no information is available on levels of parasite-specific IgT or whether these spAbs can be found in circulation, as IgT has been described mainly as a mucosal Ig (20).…”

Section: Discussionmentioning

confidence: 99%

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Passive Immunization Delays Disease Outcome in Gilthead Sea Bream Infected With Enteromyxum leei (Myxozoa), Despite the Moderate Changes in IgM and IgT Repertoire

Picard‐Sánchez

Estensoro

Perdiguero³

et al. 2020

Front. Immunol.

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Disruption of gut integrity and permeability contributes to enteritis in a fish-parasite model: a story told from serum metabolomics

Cited by 27 publications

References 100 publications

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Passive Immunization Delays Disease Outcome in Gilthead Sea Bream Infected With Enteromyxum leei (Myxozoa), Despite the Moderate Changes in IgM and IgT Repertoire

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