Epidermal Microbiomes of Leopard Sharks (Triakis semifasciata) Are Consistent across Captive and Wild Environments

Abstract

Characterizations of shark-microbe systems in wild environments have outlined patterns of species-specific microbiomes; however, whether captivity affects these trends has yet to be determined. We used high-throughput shotgun sequencing to assess the epidermal microbiome belonging to leopard sharks (Triakis semifasciata) in captive (Birch Aquarium, La Jolla California born and held permanently in captivity), semi-captive (held in captivity for <1 year in duration and scheduled for release; Scripps Institute of Oceanography, San Diego, CA, USA) and wild environments (Moss Landing and La Jolla, CA, USA). Here, we report captive environments do not drive epidermal microbiome compositions of T. semifasciata to significantly diverge from wild counterparts as life-long captive sharks maintain a species-specific epidermal microbiome resembling those associated with semi-captive and wild populations. Major taxonomic composition shifts observed were inverse changes of top taxonomic contributors across captive duration, specifically an increase of Pseudoalteromonadaceae and consequent decrease of Pseudomonadaceae relative abundance as T. semifasciata increased duration in captive conditions. Moreover, we show captivity did not lead to significant losses in microbial α-diversity of shark epidermal communities. Finally, we present a novel association between T. semifasciata and the Muricauda genus as Metagenomes associated genomes revealed a consistent relationship across captive, semi-captive, and wild populations. Since changes in microbial communities is often associated with poor health outcomes, our report illustrates that epidermally associated microbes belonging to T. semifasciata are not suffering detrimental impacts from long or short-term captivity. Therefore, conservation programs which house sharks in aquariums are providing a healthy environment for the organisms on display. Our findings also expand on current understanding of shark epidermal microbiomes, explore the effects of ecologically different scenarios on benthic shark microbe associations, and highlight novel associations that are consistent across captive gradients.

Emergent community architecture despite distinct diversity in the global whale shark (Rhincodon typus) epidermal microbiome

“…The abundant core was identified by assemblying the single reads into Metagenome Assembled Genomes (MAGs). The number of MAGs characterized in our study (35 high quality) was similar to two other studies focused on shark microbiomes, one which found 54 high/medium quality MAGs from the skin surface of leopard sharks ( Triakis semifasciata ) 28 and another that found 27 MAGs from feacal samples of two shark species 29 . These abundant core microbes may be supporting microbiome architectural patterns by providing metabolic processes.…”

“…Interestingly, microbes of these taxonomic groups are commonly associated with fish mucus microbiomes 30 and may indicate a similar role in the epidermal microbiome. Flavobacteracaea MAGs were found from the epidermal microbiome of the leopard shark ( T. semifasciata) 28 , suggesting this microbial family my be a symbiont of marine fishes (bony and cartilaginous). Gene pathways in Ecogroup 1 support this groups role as skin microbiome symbionts that utilize mucus.…”

Elasmobranchs Exhibit Species-Specific Epidermal Microbiomes Guided by Denticle Topography

“…Even though each host harbored a species-specific microbiome, we did observe some common features. Most notably, the Pseudoalteromonadaceae family was dominant across all shark hosts, consistent with microbiome surveys of T. semifasciata 16 . This family of bacteria is well-known for its crucial roles in biofilm formation and the deterrence of potential microbial predator colonization 43,44 .…”

“…The epidermal microbiomes of sharks, which have densely packed denticles, are highly shared across individuals of the same species, while the epidermal microbiomes of stingray, which have sparse dermal denticles and thick mucus, are more variable, suggesting the interaction of dermal denticles and microbiome characteristics 15,16 . Thus, while microbes pervasively associated with the epidermis of fishes throughout the host's evolutionary history, describing the specific microbial species present on the skin of marine vertebrates and the host factors influencing microbiome recruitment and retainment is required.…”

“…We previously reported the principle that captive, aquatic elasmobranch species maintain a comparable epidermal microbiome to wild counterparts 16 . The nearby proximity of captive elasmobranchs sampled in this study provided an opportunity to characterize the epidermal microbiomes associated with T. semifasciata, H. francisci, and C. ventriosum populations and test whether microbial patterns in benthic shark epidermal microbiomes mirror host phylogeny and correlate with denticle morphology.…”