Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)

Abstract

Microbial transmission from parent to offspring is hypothesized to be universal in vertebrates. However, evidence for this is limited as many clades remain unexamined. Chondrichthyes, as one of the earliest–branching vertebrate lineages, provide an opportunity to investigate the phylogenetic breadth of this hypothesis. To assess the potential for bacterial transmission in an oviparous chondrichthyan, we used 16S rRNA amplicon sequencing to characterize the microbial communities associated with the skin, gill, and egg capsule of the little skate, Leucoraja erinacea, at six points during ontogeny. We identify site-specific microbiomes dominated by the bacterial phyla Proteobacteria and Bacteroidetes, a composition similar to, but distinct from, that of other chondrichthyans. Our data reveal that the skate egg capsule harbors a highly diverse bacterial community–particularly on the internal surface of the capsule–and facilitates intergenerational microbial transfer to the offspring. Embryonic skin and external gill tissues host similar bacterial communities; the skin and gill communities later diverge as the internal gills and skin denticles develop. Our study is the first exploration of the chondrichthyan microbiome throughout ontogeny and provides the first evidence of vertical transmission in this group, which may be the primary mechanism for the signature of phylosymbiosis previously observed in elasmobranchs.

The Epidermal Microbiome Within an Aggregation of Leopard Sharks (Triakis semifasciata) Has Taxonomic Flexibility with Gene Functional Stability Across Three Time-points

“…An experiment on a human skin modelled showed that mixed microbiome communities had a greater positive effect on the skin function, including the mediation of the epidermal layer thickness, reduction in the number of actively proliferating cells, and increased filaggrin expression [59], suggesting that there is a two-way interaction between the microbes and host metabolic processes. The epidermal microbiome of embryonic skates showed a dramatic change at the time of dermal denticle hardening, going from similar to other body parts prior to denticle formation to unique post denticle formation [72], supporting our hypothesis that the dermal denticles affect microbiome structure. There was no evidence of dentine, hydrolysate, or collagen degradation in the shark skin microbiome, suggesting that the microbes are not breaking down the dermal denticles, which signifies a lack of negative impact on the sharks, at least in the form of degrading the dermal denticles.…”

“…These features are consistent across the microbiome of four shark species [26,28]. The epidermal microbiome of embryonic skates showed a dramatic change at the time of dermal denticle hardening, going from similar across all body parts to a unique microbiome on the epidermis [72], confirming the effect of the dermal denticles in microbiome structure.…”