Species-specific coral microbiome assemblages support host bleaching resistance during an extreme marine heatwave

Scleractinian assemblages are threatened by marine heat waves with coral survivorship depending on host genetics and microbiome composition. We documented an extreme marine heat wave in Fiji and the response of corals in two thermally stressed reef flats. Through high-throughput amplicon sequencing of 16S and ITS rDNA phylogenetic markers, we assessed coral microbiomes (Symbiodiniaceae, prokaryotes, fungi, and Apicomplexa) of paired bleached and unbleached colonies of four common coral species representative of dominant genera in the South Pacific. While all coral species exhibited one or more pathways to bleaching resistance, harboring assemblages composed primarily of thermally tolerant photosymbionts did not always result in host bleaching resistance. Montipora and Pocillopora species, which associate with diverse Symbiodiniaceae and vertically transmit their photosymbionts, fared better than Acropora, which acquire their photosymbionts from the environment, and Porites, which associate with a narrow photosymbiont assemblage. Prokaryotic and fungal beta diversity did not differ between bleached and unbleached conspecifics, however, the relative abundance of the fungus Malassezia globosa was significantly greater in unbleached colonies of Montipora digitata. Each coral species harbored distinct assemblages of Symbiodiniaceae, prokaryotes, and Apicomplexa, but not fungi, reiterating the importance of host genetics in structuring components of its microbiome. Terrestrial fungal and prokaryotic taxa were detected at low abundance across coral microbiomes, indicating that allochthonous microbial inputs occur, but that coral microbiomes remain dominated by marine microbial taxa. Our study offers valuable insights into the microbiome assemblages associated with coral tolerance to extreme water temperatures. [Display omitted] •All four species examined hosted unique microbiome assemblages.•Host bleaching tolerance was driven by photosymbiont assemblages in some coral species, but not others.•Unbleached Montipora had a significantly greater relative abundance of the fungus Malassezia globosa.•Terrestrial fungi and prokaryotes were found in low abundance in coral microbiomes.