Geochemical factors associated with seasonal shifts in the abalone gut microbiota across urchin-barren habitats

Abstract

The collapse of kelp forests into urchin barrens is associated with changes in seawater chemistry and macroalgal food availability, but how these environmental changes affect herbivore-associated microbiota remains poorly understood. Here, we analyzed the gut microbiota of abalone (Haliotis discus hannai) collected from mild and severe barren regions along the Korean coast during winter and summer, comparing wild abalones with those from aquaculture. Using 16S rRNA amplicon sequencing together with stepwise negative controls and prevalence-based decontamination, we characterized microbiota variation in relation to sampling site, season, and geochemical factors. Gut microbiota varied significantly with sampling site and multiple geochemical parameters, and differences between wild and farmed abalones were most strongly associated with suspended particulate matter. Seasonal turnover was observed in both groups, and analyses in wild abalones indicated that seasonal microbiota shifts were more closely associated with temperature-related geochemical variation than with temperature alone. Seasonal changes included a positive association between Vibrio abundance and chemical oxygen demand and a negative association between Propionigenium abundance and dissolved oxygen. The effects of barren severity were most pronounced in summer. After accounting for site differences, severe barren regions showed distinct microbiota composition, altered microbial interactions, decreased Pseudomonadota and Verrucomicrobiota, and increased Bacteroidota. PICRUSt2-based functional prediction suggested that severity-associated differences were mainly related to carbohydrate and energy metabolism, with lower predicted carbon fixation and pyruvate metabolism and higher predicted staurosporine biosynthesis in severe barren regions. These findings indicate that seasonal geochemical dynamics and barren-associated habitat degradation are associated with variation in the abalone gut microbiota, with the strongest ecological divergence occurring in summer.