The Change of Teleost Skin Commensal Microbiota Is Associated With Skin Mucosal Transcriptomic Responses During Parasitic Infection by Ichthyophthirius multifillis

Abstract

Teleost skin serves as the first line of defense against invading pathogens, and contain a skin-associated lymphoid tissue (SALT) that elicit gut-like immune responses against antigen stimulation. Moreover, exposed to the water environment and the pathogens therein, teleost skin is also known to be colonized by diverse microbial communities. However, little is known about the interactions between microbiota and the teleost skin mucosal immune system, especially dynamic changes about the interactions under pathogen infection. We hypothesized that dramatic changes of microbial communities and strong mucosal immune response would be present in the skin of aquatic vertebrate under parasite infection. To confirm this hypothesis, we construct an infected model with rainbow trout (Oncorhynchus mykiss), which was experimentally challenged by Ichthyophthirius multifiliis (Ich). H & E staining of trout skin indicates the successful invasion of Ich and shows the morphological changes caused by Ich infection. Critically, increased mRNA expression levels of immune-related genes were detected in trout skin from experimental groups using qRT-PCR, which were further studied by RNA-Seq analysis. Here, through transcriptomics, we detected that complement factors, pro-inflammatory cytokines, and antimicrobial genes were strikingly induced in the skin of infected fish. Moreover, high alpha diversity values of microbiota in trout skin from the experimental groups were discovered. Interestingly, we found that Ich infection led to a decreased abundance of skin commensals and increased colonization of opportunistic bacteria through 16S rRNA pyrosequencing, which were mainly characterized by lose of Proteobacteria and increased intensity of Flavobacteriaceae. To our knowledge, our results suggest for the first time that parasitic infection could inhibit symbionts and offer opportunities for other pathogens' secondary infection in teleost skin.

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

“…and Supporting Information S12). Presence of pathogens in fish skin microbiome triggers host innate and adaptive immune response, including secretion of antibodies and antimicrobial peptides (Esteban, ; Kelly and Salinas, ; Zhang et al ., ). Such immune response could increase selection intensity on fish skin.…”

A continuously changing selective context on microbial communities associated with fish, from egg to fork

“…To this respect, network analysis of microbial taxa of infected fish revealed that skin microbiota associated with high louse burdens was characterized with an increase of connections between multiple pathogenic genera ( Vibrio , Flavobacterium , Tenacibaculum , Pseudomonas ) (Llewellyn et al., 2017). The decrease of skin commensals and increase of opportunistic bacteria were also observed in rainbow trout, where parasite infection led to the loss of Proteobacteria in favour of members of the Bacteroidetes phylum (Zhang et al., 2018). Parasite–microbiota interaction is bidirectional as the microbiota can alter a parasite's colonization success, replication and virulence, shifting it along the parasitism–mutualism spectrum.…”

Characterization of the skin and gill microbiomes in farmed seabass and seabream across different age groups

“…The water microbiome of shponds were signi cantly distinct and more diverse than the skin and gill microbiomes of both sh, regardless of their age. It is known that free-living microbial communities retain higher richness than host-associated communities [31], with many studies showing a higher bacterial diversity in water relative to sh skin [28,30,36,[58][59][60], gills [14,36], gut [7,15,18,21,61], stomach [36], hindgut [36] and whole larvae [22]. Although some studies in sh have shown that the microbial communities found in the water tend to be recovered in the larval gut microbiome [17,21], others have also shown that water microbiomes do not in uence directly the microbiomes of sh mucosa [7, 8, 13-15, 18, 19, 22, 28, 30, 34, 36, 58-60, 62, 63].…”

“…Previous sh studies of skin and gill microbiomes [e.g. 7,8,36,61], including seabass and seabream [71], have shown remarkable differences in microbial composition and structure across host species and tissues. Additionally, a previous study by our group [72] showed that disease and antibiotic treatment in seabass leads to asymmetrical shifts in skin and gill microbial communities.…”

“…Research on animal microbial communities (microbiomes) is growing exponentially as the link between microbiome and host health is strongly validated by emerging evidence [1][2][3][4][5][6][7][8]. Age-related uctuations in microbiomes are well studied in humans and are considered as "natural, inevitable and benign" [9].…”