Abstract
The Atlantic horseshoe crab (Limulus polyphemus) is a common marine aquarium species and model organism for research. There is potential monetary and conservation value in developing a stable captive population of horseshoe crabs, however, one major impediment to achieving captivity is a lack of knowledge regarding captive diseases. We utilized 16S rRNA gene amplicon sequencing to track changes in the microbiomes of four body locations in three wild-caught (tracked over 14 months in captivity) and three tank-acclimated (>2 years in captivity) adult L. polyphemus in a touch tank at Shark Reef Aquarium at Mandalay Bay in Las Vegas, NV. The wild population hosted diverse and distinct microbiomes on the carapace (260 ± 96 amplicon sequence variants or ASVs), cloaca (345 ± 77 ASVs), gills (309 ± 36 ASVs), and oral cavity (359 ± 37 ASVs), which were dominated by classes Gammaproteobacteria, Bacteroidia, and Alphaproteobacteria. A rapid decline in richness across all body locations was observed within 1 month of captivity, with tank-acclimated (>2 years) animals having <5% of the initial microbiome richness and a nearly completely restructured microbial community. Tank-acclimated horseshoe crabs possessed distinct microbiomes that were highly uneven and low in species richness on the carapace (31 ± 7 ASVs), cloaca (53 ± 19 ASVs), gills (17 ± 2 ASVs), and oral cavity (31 ± 13 ASVs). The carapace, oral cavity, and gills of the tank-acclimated animals hosted abundant populations of Aeromonas (>60%) and Pseudomonas (>20%), both of which are known opportunistic pathogens of aquatic animals and can express chitinases, providing a plausible mechanism for the development of the carapace lesion pathology observed in this and other studies. The cloaca of the tank-acclimated animals was slightly more diverse than the other body locations with Aeromonas, Enterococcus, Shewanella, and Vagococcus dominating the community. These results provide an important baseline on the microbiomes of both wild and tank-acclimated horseshoe crabs and underscore the need to continue to investigate how native microbial populations may protect animals from pathogens.
Highlights
Perhaps the most challenging environmental change an organism can experience is when a wild individual is taken from a natural setting and held in captivity under artificial conditions as is the case in a laboratory, the pet trade, the food industry, or zoos and aquaria
Throughout the 14 months of captivity, the richness and evenness of the wild horseshoe crab microbiomes never reached the drastically low values of the tankacclimated population that was in captivity for over 2 years, which had
Changes in the microbiomes of horseshoe crabs over time in captivity includes significant loss of diversity, increasing uniqueness by body location, dynamic shifts in the most abundant taxa, and eventual development of highly uneven dysbiotic communities dominated by a few opportunistic pathogens, primarily Aeromonas and Pseudomonas
Summary
Perhaps the most challenging environmental change an organism can experience is when a wild individual is taken from a natural setting and held in captivity under artificial conditions as is the case in a laboratory, the pet trade, the food industry, or zoos and aquaria. An organism may be exposed to population densities and different species they would never encounter in natural settings, fostering novel biotic interactions (Morgan and Tromborg, 2007). This can be pronounced for aquatic organisms, such as in aquaculture or large aquaria, where high densities of a variety of host species share the same tank or have a common source of filtered water. In such artificial systems stress can lead to microbiome dysbiosis and infections by obligate or opportunistic pathogens (Llewellyn et al, 2014)
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