Microbial bioenergetics of coral-algal interactions

PeerJ. 2017 Jun 21;5:e3423. doi: 10.7717/peerj.3423. eCollection 2017.

Abstract

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.

Keywords: Bioenergetics; Coral-algal interactions; Ecosystem phase shifts; Heterotrophic microbes; Microbialization; Yield to power switch.

Grant support

This work was supported by the National Science Foundation (G00009988 to TNFR; OCE-0927415 to LWK and OISE-1243541 to FR), the Gordon and Betty Moore Foundation (GBMF3781 to FR), the Canadian Institute for Advanced Research (CIFAR) (CIFAR162307 to FR), and the Pew Foundation (PROJ28972 to FR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.