A multiomic analysis of in situ coral-turf algal interactions.

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

Diel population and functional synchrony of microbial communities on coral reefs.

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.

Microbial bioenergetics of coral-algal interactions.

Human impacts are causing ecosystem phase shifts from coral- to algal-dominated reef systems on a global scale. As these ecosystems undergo transition, there is an increased incidence of coral-macroalgal interactions. Mounting evidence indicates that the outcome of these interaction events is, in part, governed by microbially mediated dynamics. The allocation of available energy through different trophic levels, including the microbial food web, determines the outcome of these interactions and ultimately shapes the benthic community structure. However, little is known about the underlying thermodynamic mechanisms involved in these trophic energy transfers. This study utilizes a novel combination of methods including calorimetry, flow cytometry, and optical oxygen measurements, to provide a bioenergetic analysis of coral-macroalgal interactions in a controlled aquarium setting. We demonstrate that the energetic demands of microbial communities at the coral-algal interaction interface are higher than in the communities associated with either of the macroorganisms alone. This was evident through higher microbial power output (energy use per unit time) and lower oxygen concentrations at interaction zones compared to areas distal from the interface. Increases in microbial power output and lower oxygen concentrations were significantly correlated with the ratio of heterotrophic to autotrophic microbes but not the total microbial abundance. These results suggest that coral-algal interfaces harbor higher proportions of heterotrophic microbes that are optimizing maximal power output, as opposed to yield. This yield to power shift offers a possible thermodynamic mechanism underlying the transition from coral- to algal-dominated reef ecosystems currently being observed worldwide. As changes in the power output of an ecosystem are a significant indicator of the current state of the system, this analysis provides a novel and insightful means to quantify microbial impacts on reef health.