This project will investigate the coupling between primary producers and the utilization of dissolved organic matter (DOM) by marine heterotrophic microbes on coral reefs. Previous metagenomic studies of the microbial communities associated with near-pristine and degraded coral reefs demonstrated a shift from a microbial food web similar to the open ocean (Prochlorococcus spp. and SAR11-like bacteria) to a community dominated by "super-heterotrophs", most closely related to known pathogens like E. coli, Staphylococcus spp., Streptococcus spp., Enterobacter spp. and Vibrio spp. This shift is associated with a decline in coral cover and an increase in coral disease prevalence. Previous research by the investigators has also shown that dissolved organic carbon (DOC) concentrations are lower on coral reef platforms compared to measurements of offshore waters (60-80 micro M). On degraded reefs, they have observed DOC measurements as low as 30 - 40 micro M, a value similar to concentrations observed in the deep Pacific Ocean. The observation of low DOC measurements on degraded reefs is decoupled from the high abundance of macroalgae, which one might expect would raise levels of DOC through the release of photosynthate into the water column.
To explain this apparent paradox, the investigators suggest the following hypothesis: Reef degradation, and the associated phase-shifts from coral to algal dominance, leads to elevated levels of algal exudates in the water column, which allows the microbial community to utilize the standing stock of semi-labile DOC. This results in: 1) higher microbial numbers and biomass; 2) a community shift to 'super-heterotrophs', which are potential coral pathogens; and 3) lower standing stocks of DOC. This project will represent the first global, metagenomic study of coral reef microbial food webs. The sequence data will be supported by microbiological (e.g., direct counts and limited culturing), water chemistry (DOM characterization), benthic cover (diversity, cover, and coral disease prevalence), fish abundance, and physical oceanographic metadata. At the completion of this research, the PIs will have: 1) characterized the microbial communities (using metagenomics) from >100 coral reefs around the world; 2) determined how different sources of DOM (surface offshore DOM, surface inshore DOM, interstitial coral DOM and, turf algal derived DOM) vary in chemical characterization, help to structure microbial communities, and influence DOC remineralization on coral reefs; 3) determined whether reef-associated algae produce photosynthetic exudates that allow the microbial communities to degrade the semi-labile DOC; 4) correlated coral condition (i.e., cover and disease prevalence) to the quantity and quality of DOM, as well as microbial biomass, taxonomy and metabolisms, and; 5) characterized the residence time of water on the reef platform around Moorea and Kiritimati.
Broader impacts: At the broadest level, this cross-disciplinary project will identify the linkages between chemical, microbial and ecological processes in coral reef degradation and will inform management and conservation by identifying a likely mechanism of coral mortality. At the level of public outreach, the Coral Reef Multimedia Project, which displays mini-documentaries and short video clips about different aspects of coral reefs, will be expanded. Undergraduate and graduate students from SDSU and SIO will create original movies using the unedited reef video. This program will include 24 students over the three years of the grant and will upload 50+ new videos to the website. The Rohwer and Smith labs also sponsor a monthly coral discussion group, which is a forum for PhD and post-doctoral scientists to present their research. This Coral Club provides encouragement and suggestions for the researchers to move forward with their projects and has established a close link between the two major institutions conducting reef research in San Diego.
Our research project investigates the mechanism by which the increased growth of algae or seaweeds contributes to the mortality of stony corals in reef ecosystems. Previous research has provided evidence that the microbial communities inhabiting the surface of corals and the water column play a role in the degradation of coral reefs. Our overall hypothesis states that: Reef degradation and the associated phase-shifts from coral to algal dominance, leads to elevated levels of algal-derived organic exudates (i.e., carbon energy sources such as sugars) in the water column, which influences the microbial community dynamics in the water column. These conditions result in: 1) higher microbial numbers and biomass, 2) a community shift to 'super-heterotrophs', which are potential coral pathogens, and 3) lower standing stock concentrations of dissolved organic carbon. Our results provide strong evidence that human activities, such as fishing and pollution, provide algae with a competitive advantage over corals by facilitating a favorable environment for bacterial growth and resulting in microbially-mediated coral mortality. During two field campaigns to Moorea, French Polynesia, our group consisting of four labs from SDSU, SIO, and UCSB collaborated to elucidate the mechanism for microbially mediated mortality on coral reefs. First, we characterized organic exudate (referred to a dissolved organic carbon, DOC) release by the dominant benthic primary producers present on the reef as well as the utilization of this organic energy source by the resident microbes (Haas et al., 2011). The results from this study showed that all of the species of algae that we measured, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. The exudates released by algae also yielded the greatest bacterial growth; whereby turf algae produced nearly twice as much DOC per unit surface area as the other benthic producers, stimulating rapid bacterial growth and concomitant oxygen drawdown. These experiments have allowed us to generate predictive models of microbial dynamics on coral reefs. Figure 1 depicts a model generated from the microbial activity data from the Haas et al., 2011 study. Here, we predicted concentrations of organic exudates (DOC release) by different theoretical assemblages of reef primary producers and the subsequent bacterial cell growth yielded from these exudates. The benthic assemblages measured on three coral reefs are also shown. These types of models will be very important for generating predictions of reefs on a global scale and also for generating testable hypotheses. To complement the above study on microbial activity, the coral and algal-derived organic exudates were further characterized to determine the composition of sugars released by different species of primary producer. We found that the fleshy macroalgal exudates were enriched in the sugar components fucose and galactose whereas coral and coralline algal exudates were enriched the total concentration of sugars but in the same component proportions as ambient seawater (Figure 2). Rates of bacterial growth and carbon utilization were significantly higher in algal exudate treatments than in coral exudate and control incubations with each bacterial community selectively removing different sugar components. We also compared the bacterial community profiles that respond to exudates from different algal species by sequencing the 16S rRNA gene (Nelson et al., 2013). Coral exudates engendered the smallest shift in overall bacterial community structure, maintained high diversity, and enriched taxa from Alphaproteobacteria lineages containing cultured representatives with relatively few virulence factors (Hyphomonadaceae, Erythrobacteraceae). In contrast, macroalgal exudates selected for less diverse communities heavily enriched in copiotrophic Gammaproteobacteria lineages containing cultured pathogens with increased virulence factors (Vibrionaceae, Pseudoalteromonadaceae; Figure 2). We expanded our investigation on the influences of algal-derived carbon release on microbial activity to incorporate the effects of fish removal on coral reef ecosystems. Specifically, we investigated the influence of human activities on the allocation of energy amongst the fish and microbial communities on coral reefs. In this study, the microbialization score was determined for 100 reefs in the central Pacific. Here, a higher microbialization score reflects a greater contribution of energy from the microbial community. Microbialization scores were found to correlate positively with the NCEAS cumulative human impact scores at each island (Figure 3). Our findings suggest that human activities contribute to increased allocation of metabolic energy into the microbial portion of the food web which can result in greater microbial activity on these reefs.
