Microbiome dynamics in resistant and susceptible colonies throughout thermal bleaching and recovery support host specificity, phenotypic variability, but common microbial consortia modulating stress responses in different coral species in Hawai’i

Background Historically, Hawai’i has had few massive coral bleaching events, until two consecutive heatwaves elevated seawater temperatures in 2014 and 2015. Consequent mortality and thermal stress were observed in the reef systems of Kane’ohe Bay (O’ahu). Two of the dominant species exhibited a phenotypic dichotomy of either bleaching resistance or susceptibility (Montipora capitata and Porites compressa), while a third species (Pocillopora acuta) was broadly susceptible to bleaching. In order to survey temporal shifts in the coral microbiomes during bleaching and recovery in all three of these coral species, 50 colonies were tagged and periodically monitored. Metabarcoding of three genetic markers (16S rRNA gene ITS1 and ITS2) followed by compositional approaches for community structure analysis, differential abundance and correlations for longitudinal data were used to temporally track and compare Bacteria/Archaea, Fungi and Symbiodiniaceae dynamics of the tagged colonies. Results Bleaching susceptible P. compressa corals recovered faster than P. acuta and Montipora capitata. Prokaryotic and algal microbiomes were majorly shaped by host species, and had no apparent pattern of temporal acclimatization in the overall community structure. Symbiodiniaceae signatures were identified at the colony scale, and were at times related to bleaching susceptibility, revealing higher intraspecific resolution than previously reported. Bacterial compositions were practically constant between bleaching phenotypes, and more diverse in P. acuta and M. capitata. P. compressa’s prokaryotic community was dominated by a single symbiotic bacterium. Fungal associates remained unexplored due to untargeted DNA co-amplification. Compositional approaches (via microbial balances) allowed the identification of fine-scale differences in the abundance of a consortium of microbes, driving changes by bleaching susceptibility and time across all hosts. Conclusions The three major coral reef founders in Kane’ohe Bay revealed different physiological and microbiome responses after 2014–2015 heatwaves. It is difficult to forecast though, a more successful strategy towards future scenarios of global warming. Differentially abundant microbial taxa across time and/or bleaching susceptibility were broadly shared between all hosts, suggesting that locally, the same microbes may modulate stress responses in sympatric coral species. Our study highlights the potential of investigating microbial balances to identify fine-scale microbiome changes, serving as local diagnostic tools of coral reef fitness.