Near-benthic coral reef picoplankton vary at fine scales decoupled from benthic cover

Seawater microorganisms impact ecological and biogeochemical cycling on coral reefs and are sensitive indicators of ecosystem status. Microbialization, a shift towards trophic collapse and resultant high microbial biomass, is a global concern on coral reefs. Indeed, macroorganisms can influence microbial processes and community composition on reefs, which is best understood as increased macroalgae resulting in copiotrophic microbial growth and oxygen reduction. Whether or not smaller-scale changes in macroorganisms influence the overlying seawater microbial communities is largely unknown. Here, we assessed seawater microorganisms across 3 coral reefs to understand their connection to reef site and within-reef benthic characteristics. At 3 coral reefs in St. John, US Virgin Islands, we collected 60 ml seawater samples 2 cm above the seafloor, spaced 2 m apart in a grid pattern, and assessed bacterial and archaeal communities via sequencing of small subunit ribosomal RNA genes. Benthic cover within 1 m of each sample was determined at 10 cm resolution through photogrammetry. Our results reveal that overall reef site overwhelmingly shapes microbial community structure, while within-reef benthic cover surrounding sample locations has minimal influence. However, ecospheres as areas that reflect the small-scale effects of benthic cover directly under each sample, significantly explain as much as 12.1% of within-reef microbial variation and may even outweigh variation attributable to reef site alone. These findings provide new insights into fine-scale spatial variability in reef seawater microbiomes that are crucial for the use of microorganisms as indicators of microbialization and coral reef health.