Microbial predictors of environmental perturbations in coral reef ecosystems

Abstract

Incorporation of microbial community data into environmental monitoring programs could improve prediction and management of environmental pressures. Coral reefs have experienced dramatic declines due to cumulative impacts of local and global stressors. Here we assess the utility of free-living (i.e. seawater and sediment) and host-associated (i.e. corals, sponges and macroalgae) microbiomes for diagnosing environmental perturbation based on their habitat-specificity, environmental sensitivity and uniformity. We show that the seawater microbiome has the greatest diagnostic value, with environmental parameters explaining 56% of the observed compositional variation and temporal successions being dominated by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less affected by the environment and their community assembly patterns were generally less uniform. Further, seawater microbial community data provided an accurate prediction on the environmental state, highlighting the diagnostic value of microorganisms and illustrating how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater.\n\nImportanceThe recent success in disease diagnostics based on the human microbiome has highlighted the utility of this approach for model systems. However, despite improved prediction and management of environmental pressures from the inclusion of microbial community data in monitoring programs, this approach has not previously been applied to coral reef ecosystems. Coral reefs are facing unprecedented pressure on a local and global scale, and sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. In this study, we performed the first assessment of the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems. Our results reveal that free-living microbial communities have a higher potential to infer environmental parameters than host-associated microbial communities due to their higher determinacy and environmental sensitivity. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.