Reshuffling of the coral microbiome during dormancy

Abstract

Quiescence, or dormancy, is a response to stressful conditions in which an organism slows or halts physiological functioning. Although most species that undergo dormancy maintain complex microbiomes, there is little known about how dormancy influences and is influenced by the hosts microbiome, including in the temperate coral, Astrangia poculata. Northern populations of A. poculata undergo winter quiescence. Here, we characterized wild A. poculata microbiomes in a high-resolution sampling time series before, during, and after quiescence using 16S ribosomal RNA gene sequencing on active (RNA) and present (DNA) microbiomes. We observed a restructuring of the coral microbiome during quiescence that persisted after re-emergence. Upon entering quiescence, corals shed copiotrophic microbes, including putative pathogens, suggesting removal of these taxa as corals cease normal functioning. During and after quiescence, bacteria and archaea associated with nitrification were enriched, suggesting the quiescent microbiome may replace essential functions through supplying nitrate to corals and/or microbes. Overall, this study demonstrates that key microbial groups related to quiescence in A. poculata may play a role in the onset or emergence from dormancy, and long-term regulation of the microbiome composition. The predictability of dormancy in A. poculata provides an ideal natural manipulation system to further identify factors that regulate host-microbial associations. ImportanceUsing a high-resolution sampling time series, we are the first to demonstrate a persistent microbial community shift with quiescence (dormancy) in a marine organism, the temperate coral, Astrangia poculata. Furthermore, during this period of community turnover, there is a shedding of putative pathogens and copiotrophs and an enhancement of the ammonia-oxidizing bacteria (Nitrosococcales) and archaea (Ca. Nitrosopumilus). Our results suggest that quiescence represents an important period during which the coral microbiome can "reset," shedding opportunistic microbes and enriching for the re-establishment of beneficial associates, including those that may contribute nitrate while the coral animal is not actively feeding. We suggest this work provides foundational understanding of the interplay of microbes and the hosts dormancy response in marine organisms.