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

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.

Microbial Interactions with Dissolved Organic Matter Are Central to Coral Reef Ecosystem Function and Resilience

“…These biogeochemical influences enrich distinct microbial taxa in reefs relative to the ocean, a pattern demonstrated in reefs across the globe (Frade et al 2020, McCliment et al 2012, Weber et al 2020b. Additionally, inputs of microbes from land sources (e.g., streams, runoff, and groundwater) and from the microbiomes of the diverse fauna that make up the benthic community further influence microbial signatures in reef environments (Quinlan et al 2019, Remple et al 2021, Wilkins et al 2019.…”

“…Bioturbation and digestion by various invertebrate scavengers ensure that the sand does not accumulate decomposing organic matter, limiting the successional stagnation of the biofilms (Williamson et al 2021). Biofilm structure and function in reefs are driven largely by the composition of benthic exudates released locally (Remple et al 2021) and in this way may link the benthic producers and invertebrate consumers through the structure and function of sand biofilm communities.…”

Biofilms as potential reservoirs of stony coral tissue loss disease

“…Hypothesizing that these more "polluted" conditions represent more nutrient-rich environments for microbial growth, blooms of opportunistic prokaryotes responding to localized nutrient-enrichment may at least partially explain some of the differences that we observed between microbial biofilms associated with apparently healthy and SCTLD-infected corals. Nutrient enrichment has previously been shown to significantly influence marine biofilm microbial communities, though not as much as other variables such as exposure to different macroorganisms (Remple et al, 2021). However, looking exclusively at biofilms formed in association with corals, Remple et al (2021) found that nutrient enrichment resulted in an increase in species richness and a decrease in species evenness, as well as increases in Flavobacteriaceae, a family which was considerably more enriched in diseased compared to healthy mesocosms (average n = ~4,260 and 121 reads, respectively) and which we do see represented within our SCTLD-obligate-andspecific ASVs (ASVs 35 and 236).…”

“…Nutrient enrichment has previously been shown to significantly influence marine biofilm microbial communities, though not as much as other variables such as exposure to different macroorganisms (Remple et al, 2021). However, looking exclusively at biofilms formed in association with corals, Remple et al (2021) found that nutrient enrichment resulted in an increase in species richness and a decrease in species evenness, as well as increases in Flavobacteriaceae, a family which was considerably more enriched in diseased compared to healthy mesocosms (average n = ~4,260 and 121 reads, respectively) and which we do see represented within our SCTLD-obligate-andspecific ASVs (ASVs 35 and 236). This suggests that the apparent water quality deterioration observed in some diseased mesocosms may indeed have resulted in a nutrient shift that impacted the resulting mesocosm and biofilm microbial communities.…”

“…Given the apparent waterborne transmission route of SCTLD (Aeby et al, 2019;Dobbelaere et al, 2020;Muller et al, 2020), the unknown pathogen(s) must be shed by infected corals into the surrounding water. It has been established that biofilm community composition may be influenced by the close proximity of benthic organisms, including corals (Remple et al, 2021). It therefore seems reasonable that the causative agent of SCTLD could join a biofilm microbial assemblage.…”