Coral reef biofilm bacterial diversity and successional trajectories are structured by reef benthic organisms and shift under chronic nutrient enrichment

Kristina L Remple,Zachary A Quinlan,Megan J Donahue,Craig E Nelson,Nyssa J Silbiger,Linda Wegley Kelly,Michael D Fox

doi:10.1038/s41522-021-00252-1

Abstract

Work on marine biofilms has primarily focused on host-associated habitats for their roles in larval recruitment and disease dynamics; little is known about the factors regulating the composition of reef environmental biofilms. To contrast the roles of succession, benthic communities and nutrients in structuring marine biofilms, we surveyed bacteria communities in biofilms through a six-week succession in aquaria containing macroalgae, coral, or reef sand factorially crossed with three levels of continuous nutrient enrichment. Our findings demonstrate how biofilm successional trajectories diverge from temporal dynamics of the bacterioplankton and how biofilms are structured by the surrounding benthic organisms and nutrient enrichment. We identify a suite of biofilm-associated bacteria linked with the orthogonal influences of corals, algae and nutrients and distinct from the overlying water. Our results provide a comprehensive characterization of marine biofilm successional dynamics and contextualize the impact of widespread changes in reef community composition and nutrient pollution on biofilm community structure.

Highlights

IntroductionBiofilms are complex communities of surface attached microorganisms that are encased in an extracellular polymeric matrix[1]
Biofilms are complex communities of surface attached microorganisms that are encased in an extracellular polymeric matrix[1].They are ubiquitous in aquatic environments where they provide ecosystem services including primary production[2], organic matter decomposition[3], and nutrient cycling[4]
We demonstrate that biofilms exhibit a successional trajectory that diverges from the stochastic temporal dynamics of

Summary

Introduction

Biofilms are complex communities of surface attached microorganisms that are encased in an extracellular polymeric matrix[1] They are ubiquitous in aquatic environments where they provide ecosystem services including primary production[2], organic matter decomposition[3], and nutrient cycling[4]. Studies focusing on bacterioplankon communities on coral reefs have revealed active and dynamic heterotrophic bacterial assemblages influenced by reef residence time[13,14,15], diel ecosystem processes[16], sources and concentrations of organic matter[13,17,18], reef benthic composition[19,20,21,22], direct coral interactions[23,24], and nutrient availability[20,21]. Populations of potentially pathogenic bacteria and virulence genes increase in the surface mucus layer of corals in response to increased nutrient loads[25,26]; and the microbiomes of physiologically sensitive corals may experience an overall decrease in microbial diversity accompanied by an increase in diseaseassociated microbes with ocean acidification and warming[27]

Methods

Results

Conclusion