Parasitism perturbs the mucosal microbiome of Atlantic Salmon

Abstract

Interactions between parasite, host and host-associated microbiota are increasingly understood as important determinants of disease progression and morbidity. Salmon lice, including the parasitic copepod Lepeophtheirus salmonis and related species, are perhaps the most important problem facing Atlantic Salmon aquaculture after feed sustainability. Salmon lice parasitize the surface of the fish, feeding off mucus, scales and underlying tissue. Secondary bacterial infections are a major source of associated morbidity. In this study we tracked the diversity and composition of Salmo salar skin surface microbiota throughout a complete L. salmonis infection cycle among 800 post-smolts as compared to healthy controls. Among infected fish we observed a significant reduction in microbial richness (Chao1, P = 0.0136), raised diversity (Shannon, P < 7.86e-06) as well as highly significant destabilisation of microbial community composition (Pairwise Unifrac, beta-diversity, P < 1.86e-05; P = 0.0132) by comparison to controls. While undetectable on an individual level, network analysis of microbial taxa on infected fish revealed the association of multiple pathogenic genera (Vibrio, Flavobacterium, Tenacibaculum, Pseudomonas) with high louse burdens. We discuss our findings in the context of ecological theory and colonisation resistance, in addition to the role microbiota in driving primary and secondary pathology in the host.

Composition of the microbial communities in the gastrointestinal tract of perch (Perca fluviatilis L. 1758) and cestodes parasitizing the perch digestive tract

“…I G U R E 5 Predicted functional metagenomic pathways for stomach and intestinal mucosa and content of perch and cestodes at levels 2 and 3. Blue, stomach mucosa; violet, stomach content; green, pyloric caeca; red, intestinal mucosa; light blue, intestinal content; orange, cestodes [Colour figure can be viewed at wileyonlinelibrary.com] genera such as Vibrio, Flavobacterium, Tenacibaculum and Pseudomonas(Llewellyn et al, 2017).As shown earlier in this study, the microbiota associated with Proteocephalus sp. extracted from perch in Chany Lake was dominated by bacteria from the genera Serratia, Pseudomonas and Mycoplasma, unidentified bacteria from the family Enterobacteriaceae and Bacillus, and unclassified clade u114 from the family Fusobacteriaceae.…”

“…Bacteria associated with parasites isolated from fish have been most extensively studied and are known to belong to a wide range of microbial taxa (Hughes‐Stamm et al, ; Korneva & Plotnikov, ; Llewellyn et al, and others). Parasite‐associated microbiota has been described for Monogenea, Trematoda, Cestoda, Nematoda and Crustacea (Table S3 and Table S4).…”

“…that may act as vectors for pathogenic aeromonads and being almost ubiquitous on salmonid fish may be a prominent reservoir for Aeromonas infections (Cusack & Cone, ). The study regarding the diversity and composition of Salmo salar microbiota parasitized on their skin by the copepod Lepeophtheirus salmonis has revealed the association of multiple, potentially pathogenic bacterial genera such as Vibrio , Flavobacterium , Tenacibaculum and Pseudomonas (Llewellyn et al, ).…”

Environmental conditions and neutral processes shape the skin microbiome of European catfish (Silurus glanis) populations of Southwestern France

“…; Llewellyn et al . ). Given the high number of freshwater fish species existing worldwide and belonging to very contrasted phylogenetic lineages (Nelson, Grande and Wilson ), the description of skin microbiome of phylogenetically contrasted fish species appears necessary for drawing better predictions of skin microbiome variability among freshwater fishes.…”

Using fish models to investigate the links between microbiome and social behaviour: The next step for translational microbiome research?

“…Disentangling the links between microbiome and fish health is a hot topic, particularly given the growth of the aquaculture industry. In this respect, the effects of pathogens, antibiotics and probiotics on microbiome composition have been subject of several studies showing that significant changes take place (e.g., Carlson, Leonard, Hyde, Petrosino, & Primm, 2017;Gonçalves & Gallardo-Escarate, 2017;Hennersdorf et al, 2016;Li et al, 2016;Llewellyn et al, 2017;Reid et al, 2017).…”