Bacterial community dynamics are linked to patterns of coral heat tolerance

Abstract

Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.

Figure 1. Long-term transplantation and short-term heat stress experiment.

(a) View of the back reef pool locations (HV and MV pool) on American Samoa, and sampling design of the reciprocal transplantation experiment of fragmented colonies of Acropora hyacinthus between the pools; (b) temperature profiles measured in the HV (black) and MV (grey) pools over time (modified following Oliver and Palumbi24) and short-term heat stress experiment and sampling; (c) non-metric Multidimensional Scaling (nMDS) of bacterial community composition after transplantation between HV and MV pools; each symbol represents a sample, symbol shapes denote pool of origin (circles=HV pool, triangles=MV pool), symbol colours denote pool of destination (orange=HV pool, blue=MV pool), ellipses are drawn around each group's centroid; ellipse lines: dashed for cross-transplants, continuous for back-transplants, filled ellipse for significant pool-of-destination groups (ANOSIM, R=0.122, P<0.001); (d) 16S rRNA sequence-based microbial community composition of reciprocally transplanted colonies between HV and MV pool locations on the bacterial family level. Differentially abundant bacterial families between the two pools are marked with an ‘*' if more abundant in the HV pool and with a ‘+' if more abundant in the MV pool. HV, highly variable pool, MV, moderately variable pool, 05C and 20C=5 and 20 h control (C) short-term heat stress experiment, 05H and 20H=5 and 20 h treatment (H) short-term heat stress experiment. Sample name scheme in (c,d): ‘pool-of-origin.pool-of-destination.time (05=5 h, 20=20 h) treatment (C=control, H=heat)' in short-term heat stress experiment.

Figure 2. Bacterial indicator taxa of coral thermal environments and heat stress tolerance.

(a) Abundance of bacterial indicator taxa that characterize heat-tolerant corals in the HV pool over all treatments of the short-term heat stress experiment. (b) Abundance of bacterial indicator taxa that characterize the heat stress response in heat-sensitive corals in the MV pool. Each cell represents the square root transformed mean count of each indicator OTU per group (n=10–13). Previous occurrences of identical or highly similar bacteria are listed with their environmental source and GenBank Accession number. HV, highly variable pool; MV, moderately variable pool; 05C and 20C=5 and 20 h control (C) short-term heat stress experiment; 05H and 20H=5 and 20 h treatment (H) short-term heat stress experiment.