Abstract
BackgroundUnderstanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiome associations are beneficial, yet the mechanisms that determine the composition of the coral microbiome remain largely unknown. Here, we characterized microbiome diversity in the temperate, facultatively symbiotic coral Astrangia poculata at four seasonal time points near the northernmost limit of the species range. The facultative nature of this system allowed us to test seasonal influence and symbiotic state (Symbiodinium density in the coral) on microbiome community composition.ResultsChange in season had a strong effect on A. poculata microbiome composition. The seasonal shift was greatest upon the winter to spring transition, during which time A. poculata microbiome composition became more similar among host individuals. Within each of the four seasons, microbiome composition differed significantly from that of surrounding seawater but was surprisingly uniform between symbiotic and aposymbiotic corals, even in summer, when differences in Symbiodinium density between brown and white colonies are the highest, indicating that the observed seasonal shifts are not likely due to fluctuations in Symbiodinium density.ConclusionsOur results suggest that symbiotic state may not be a primary driver of coral microbial community organization in A. poculata, which is a surprise given the long-held assumption that excess photosynthate is of importance to coral-associated microbes. Rather, other environmental or host factors, in this case, seasonal changes in host physiology associated with winter quiescence, may drive microbiome diversity. Additional studies of A. poculata and other facultatively symbiotic corals will provide important comparisons to studies of reef-building tropical corals and therefore help to identify basic principles of coral microbiome assembly, as well as functional relationships among holobiont members.
Highlights
Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats
Symbiotic states have previously been assigned according to color and approximated chlorophyll concentration [32, 35, 36] and cell density of Symbiodinium in summer months [37], with brown colony Symbiodinium densities exceeding 106 cells cm−2 coral tissue, and white colony Symbiodinium densities ranging from 104 to 106 cells cm−2 [37]. By sampling both across seasons and across colonies varying in symbiotic state, our objective is to determine whether the taxonomic structure of the microbiome in A. poculata is linked to symbiotic state or to other factors that fluctuate seasonally
Here, the facultative nature of the A. poculata-S. psygmophilum symbiosis has enabled us to distinguish the role of season from the role of symbiosis in structuring the coral microbiome
Summary
Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Sharp et al Microbiome (2017) 5:120 include variation in the host’s physiology (e.g., due to developmental stage), the activity and abundance of host-associated Symbiodinium, and the chemical and physical properties of the surrounding environment, with all of these potentially linked to both natural (seasonal) and anthropogenic changes in ocean conditions. Bleaching, which involves loss of intracellular photosynthetic Symbiodinium, triggers rapid changes in physiological interactions in tissue, skeleton, and mucus layers, with observed taxonomic and genomic changes in the coral microbiome [19, 26, 27]. In tropical corals, sustained warming events and resultant loss of Symbiodinium (bleaching) have been shown to result in a decrease in defensive properties of coral mucus and bioactivity against known coral pathogens [7], potentially allowing for infection and disease [9, 28]. It is crucial to assemble a model of microbe-microbe interactions within the coral meta-organism that can describe the relative roles of Symbiodinium versus environmental conditions, such as temperature, as drivers of prokaryotic diversity
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