From sediment to coral symbionts: persistent spatial structure across reef microbiomes

Abstract

Environmental context can structure microbial communities across space and time, but it remains unclear whether these patterns extend across free-living and host-associated communities or how they interact with host genetic background. We explored these relationships in reef sediments and the reef-building coral Orbicella faveolata in St. Croix, US Virgin Islands. We first repeatedly sampled sediments and individual coral colonies at two reefs over three weeks to compare microbial and algal symbiont (Symbiodiniaceae) communities between reefs and through time. Sediment microbial communities differed strongly between reefs and changed over the three-week period. Their functional composition showed similar patterns, indicating that taxonomic changes were accompanied by shifts in functional potential. In contrast, Symbiodiniaceae communities in both reef sediments and repeatedly sampled coral colonies differed strongly between reefs but remained largely stable through time. We then expanded our analysis across St. Croix to test whether host genetic differences could explain spatial variation in coral-associated Symbiodiniaceae. Symbiodiniaceae composition varied strongly among sites and with depth but was not associated with the two known genetic groups of O. faveolata. Together, these results show that components of the reef microbiome differ in their temporal dynamics but share strong spatial structure. While sediment microbial communities changed over just three weeks, Symbiodiniaceae communities were comparatively stable through time, and spatial differences among coral-associated Symbiodiniaceae persisted across the island regardless of host genetic background. Thus, reef site emerges as a strong and persistent source of variation across both free-living and host-associated components of the reef microbiome.