The effects of feeding guild, seasonality, and warming on the gut microbiomes of Antarctic echinoderms

BACKGROUND: Antarctic marine food webs are expected to be significantly impacted by future climate change. In particular, the recent rapid regional warming in the West Antarctic Peninsula has, and will continue to have, a negative impact on endemic marine biodiversity. However, despite the growing recognition of the role microbial symbionts play in mediating responses to environmental change, microbiome characterisation has been conducted for only a small fraction of the marine invertebrates in the Southern Ocean. Our study examined the effects of feeding guild, seasonality, and experimental warming (6 months at + 2 °C) on the gut microbiome of six species of near-shore marine Antarctic echinoderms sampled from waters off Rothera Research Station, Antarctica. Our study used 16 S rRNA amplicon sequencing of the V3-V4 region, with analyses including measurements of alpha and beta-diversity alongside co-occurrence network analyses. RESULTS: Of the six invertebrate species sampled in winter, peak species diversity values in gut microbiomes were observed in the omnivores, Ophionotus victoriae and Sterechinus neumayeri, with lower values in the scavenger/predator, Odontaster validus, and the suspension feeders, Cucumaria georgiana, Echinopsolus charcoti, and Heterocucumis steineni. In the seasonal experiment, H. steineni bacterial gut species diversity doubled from winter to early summer yet decreased by a similar magnitude during the same period in O. victoriae. Despite these opposing diversity trends, both species displayed similar increases in the relative abundances of Bacteroidota and Bacillota in winter and early summer in their gut microbiomes. Bacterial diversity in the gut microbiome of the sea cucumbers E. charcoti and H. steineni, was not impacted by six-months at + 2 ˚C above ambient, although C. georgiana displayed a decrease in observed ASVs following this treatment. CONCLUSIONS: These results suggest a strong influence of feeding guild and seasonality on the gut microbiomes of these invertebrates. There appeared to be little effect of warming (+ 2 °C) on the taxonomic composition of the gut microbiomes of the three holothurians. This highlights the need to examine the functional significance of experimental warming treatments using metabolomics and transcriptomics alongside microbial species diversity analyses to understand whether gut microbiomes can aid resilience under future climate change.