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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.

The rapidly advancing field of metabolomics encompasses a diverse suite of powerful analytical and bioinformatic tools that can help to reveal the diversity and activity of chemical compounds in individual organisms, species interactions, and entire ecosystems. In this perspective we use examples from studies of coral reefs to illustrate ways in which metabolomics has been and can be applied to understand coastal ecosystems. Examples of new insights that can be provided by metabolomics include resolving metabolite exchange between microbes and animals in holobiont tissues, identifying the relevant metabolite exchanges associated with the onset and maintenance of diverse bacterial endosymbionts, characterizing unknown molecules associated with coral reproductive cues, or defining the suites of compounds involved in coral-algal competition and microbialization of algal-dominated ecosystems. Here we outline sampling, analytical and informatic methods that marine biologists and ecologists can apply to understand the role of chemical processes in ecosystems, with a focus on open access data analysis workflows and democratized databases. This perspective aims to demonstrate that metabolomics tools and bioinformatics approaches which leverage open access chemical databases can provide scientists the opportunity to map detailed metabolic inventories and dynamics for a holistic view of the relationships among reef organisms, their symbionts and their surrounding marine environment.

All organisms host a diversity of associated viruses, bacteria, and protists, collectively defined as the holobiont. While scientific advancements have enhanced the understanding of the functional roles played by various components of the holobiont, there is a growing need to integrate multiple types of molecular data into spatially and temporally resolved frameworks. To that end, we mapped 16S and 18S rDNA metabarcoding, metatranscriptomics, and metabolomic data onto three-dimensional reconstructions of coral colonies to examine microbial diversity, microbial gene expression, and biochemistry on two colonies of the ecologically important, reef-building coral,Orbicella faveolataand their competitors (i.e., adjacent organisms interacting with the corals: fleshy algae, turf algae, hydrozoans, and other corals). Overall, no statistically significant spatial patterns were observed among the samples for any of the data types; instead, strong signatures of the macroorganismal hosts (e.g., coral, algae, hydrozoa) were detected, in the microbiome, the transcriptome, and the metabolome. The 16S rDNA analysis demonstrated higher abundance of Firmicutes in the coral microbiome than in its competitors. A single bacterial amplicon sequence variant from the genusClostridiumwas found exclusively in allO. faveolatasamples. In contrast to microbial taxa, a portion of the functionally annotated bacterial RNA transcripts (6.86%) and metabolites (1.95%) were ubiquitous in all coral and competitor samples. Machine learning analysis of microbial transcripts revealed elevated T7-like cyanophage-encoded photosystem II transcripts inO. faveolatasamples, while sequences involved in bacterial cell division were elevated in turf algal and interface samples. Similar analysis of metabolites revealed that bacterial-produced antimicrobial and antifungal compounds were highly enriched in coral samples. This study provides insight into the spatial and biological patterning of the coral microbiome, transcriptome, and metabolome.

Dissolved organic matter (DOM) composition is a key determinant of microbial community metabolism and trophic nutrient transfer. On coral reefs, four primary groups of benthic organisms dominate photosynthetic production: corals, macroalgae, microphytobenthos, and encrusting algae on rubble, all of which exude significant quantities of DOM. We conducted a mesocosm experiment to characterize and contrast DOM exudates from these four organismal groups under three levels of continuous inorganic nutrient enrichment. We measured bulk dissolved organic carbon and nitrogen and the multivariate spectral characteristics of fluorescent DOM (fDOM). Moderate nutrient enrichment enhanced DOM exudation by all producers. Corals exuded rapidly accumulating DOM with a markedly high concentration of aromatic amino acid-like fDOM components that clearly distinguishes them from algal exudates, which were dominated by humic-like fDOM components and did not accumulate significantly. Our results emphasize the differences between coral and algae in their potential to influence microbial communities and metabolism in reefs.

Crustose coralline algae (CCA) are critical members of the coral reef ecosystem, yet they remain poorly studied. Recent research on CCA has shown that only a few species play a significant role in the settlement of coral larvae through either the production of chemical settlement cues or the facilitation of specific microbial communities that are hypothesized to influence coral settlement. Thus, defining how DOM exudates differ between CCA species and the bacterioplankton communities these exudates facilitate is important for understanding the role of CCA in invertebrate settlement. We conducted single day exudation experiments on two species of CCA to compare tissue microbiome community structure, DOM production and the effect of DOM on the bacterioplankton community. We collected exudates from Hydrolithon reinboldii and Porolithon onkodes in both filter-sterilized seawater and unfiltered seawater from Kāne‘ohe Bay, Hawai‘i. Our results demonstrate that while both species exude equivalent quantities of dissolved organic carbon they differ in the composition of fluorescent DOM and fostered distinct microbial communities. P. onkodes exudates facilitate more microbial OTUs associated with coral disease, whereas H. reinboldii facilitated OTUs known to produce antimicrobial compounds. Our results highlight species-specific differences in the composition of fDOM exudates of CCA and the effect of those on microbial community structure.

On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs., Microbes structure biogeochemical cycles and food webs in the marine environment. Here, the authors sample coral reef-associated microbes across a 24-hour period, showing clear day–night patterns of microbial populations and thus calling for more studies to consider temporal variation in microbiomes at this scale.