Hidden microalgae diversity in reef systems: reanalysis of coral microbiomes reveals spatial patterns of coral-associated plastid communities in the Southwestern Atlantic Ocean (SWAO)

The microbial community associated with corals plays a critical role in reef ecosystems, yet studies mainly focus on prokaryotes and Symbiodiniaceae, overlooking other oxygen-evolving photosynthetic eukaryotes. This leaves a knowledge gap regarding potentially important microbiome members. Here, we revisited coral microbiome datasets to investigate the diversity of plastid-bearing eukaryotes associated with Southwestern Atlantic Ocean (SWAO) corals. We compiled an inventory of plastid-bearing communities, uncovering their diversity and exploring ecological patterns. We further applied this approach to analyze the plastidiomes (plastid-bearing communities) of corals from the Abrolhos Bank, the largest reef system in the region, as a case study. A systematic literature review of 16S rDNA-based coral microbiome was conducted, excluding studies lacking plastid 16S sequences. The search made in PubMed resulted in 19 studies reporting corals sampled from 2009 to 2022, which were compiled and reanalyzed. Sequences of chloroplast origin (Silva 132) were further taxonomically classified by consensus-<i>BLASTn</i> search with the PR2 plastid 16S database. The dataset encompassed reef water and coral microbiomes from eight coral species, emphasizing the genus <i>Mussismilia</i>. A total of 272 amplicon libraries yielded 707,949 plastid sequences, identifying 196 algal genera across 41 classes. Reef water and coral plastid communities differed markedly. <i>Ostreobium</i> (81%) and <i>Calliarthron</i> (49%) were the most prevalent genera in coral samples. Diatoms were common (>40% of samples) in the water and in corals, whereas corallicolids were exclusive to corals (31.8%). The Abrolhos case study revealed geographic variation in <i>Mussismilia harttii</i> plastidiomes, which were less diverse than those in the water column. Coral indicator taxa included <i>Ostreobium</i>, corallicolids, <i>Navicula</i>, and <i>Amphora</i>. Our findings identify plastidiome variations and their implications for the coral host. Lipid-rich diatoms prevalent in coral plastidiomes may support corals nutritionally after coral bleaching, while other free-living and bloom-forming microalgae produce significantly more reactive oxygen species than Symbiodiniaceae, potentially driving oxidative stress. These results highlight microeukaryotic community variation across corals and its ecological relevance, offering a framework for using plastid-bearing communities as biomarkers of shifts in coral holobionts.