Gene content of seawater microbes is a strong predictor of water chemistry across the Great Barrier Reef.

Background: Seawater microbes (bacteria and archaea) play essential roles in coral reefs by facilitating nutrient cycling, energy transfer, and overall reef ecosystem functioning. However, environmental disturbances such as degraded water quality and marine heatwaves, can impact these vital functions as seawater microbial communities experience notable shifts in composition and function when exposed to stressors. This sensitivity highlights the potential of seawater microbes to be used as indicators of reef health. Microbial indicator analysis has centered around measuring the taxonomic composition of seawater microbial communities, but this can obscure heterogeneity of gene content between taxonomically similar microbes, and thus, microbial functional genes have been hypothesized to have more scope for predictive potential, though empirical validation for this hypothesis is still pending. Using a metagenomics study framework, we establish a functional baseline of seawater microbiomes across offshore Great Barrier Reef (GBR) sites to compare the diagnostic value between taxonomic and functional information in inferring continuous physico-chemical metrics in the surrounding reef.

Results: Integrating gene-centric metagenomics analyses with 17 physico-chemical variables (temperature, salinity, and particulate and dissolved nutrients) across 48 reefs revealed that associations between microbial functions and environmental parameters were twice as stable compared to taxonomy-environment associations. Distinct seasonal variations in surface water chemistry were observed, with nutrient concentrations up to threefold higher during austral summer, explained by enhanced production of particulate organic matter (POM) by photoautotrophic picocyanobacteria, primarily Synechococcus. In contrast, nutrient levels were lower in winter, and POM production was also attributed to Prochlorococcus. Additionally, heterotrophic microbes (e.g., Rhodospirillaceae, Burkholderiaceae, Flavobacteriaceae, and Rhodobacteraceae) were enriched in reefs with elevated dissolved organic carbon (DOC) and phytoplankton-derived POM, encoding functional genes related to membrane transport, sugar utilization, and energy metabolism. These microbes likely contribute to the coral reef microbial loop by capturing and recycling nutrients derived from Synechococcus and Prochlorococcus, ultimately transferring nutrients from picocyanobacterial primary producers to higher trophic levels.

Conclusion: This study reveals that functional information in reef-associated seawater microbes more robustly associates with physico-chemical variables than taxonomic data, highlighting the importance of incorporating microbial function in reef monitoring initiatives. Our integrative approach to mine for stable seawater microbial biomarkers can be expanded to include additional continuous metrics of reef health (e.g., benthic cover of corals and macroalgae, fish counts/biomass) and may be applicable to other large-scale reef metagenomics datasets beyond the GBR. Video Abstract.