Craig E. Nelson

Coral reefs are biodiverse and productive ecosystems that are found in typically oligotrophic environments. Many studies have attempted to explain this paradox by demonstrating that microbial symbionts expand metabolic capabilities of host animals. However, few studies have determined if and how coexisting organisms and their symbiotic microbial communities partition available dissolved organic matter. To address this question, we built an artificial reef near the Florida Keys using dominant emergent sponges found in the Caribbean. Fluorescent dissolved organic matter (fDOM) components were measured in incurrent and excurrent water samples of 5–7 biological replicates for each of 10 sponge species. Sponges generally consumed more fDOM as incurrent concentrations increased, but there were also species‐level differences in their responses. We found that microbial abundance (i.e., high and low microbial abundance HMA/LMA classification) explained less variation in fDOM processing than sponge species. Additionally, fDOM analysis revealed both a separation of sponges into two groups based on whether they were net producers or consumers of fDOM, as well as their responses to fDOM concentrations in ambient seawater across species. Differential consumption of fDOM components also yielded species‐specific fluxes of fDOM. This observation contrasts with broad uptake of all fDOM components, which would be expected if net consumption of fDOM was simply concentration dependent and the same for all species. These results provide the first support for species‐level resource partitioning of fluorescent dissolved organic matter across coexisting sponge species and provide additional support for the evolutionary importance of microbial communities in sponges.

Local-scale nutrient input from seabird guano and human wastewater are hypothesized to enhance and hinder coral performance, respectively, with seabird guano possibly mitigating heat stress. To test this hypothesis, we compared the effects of anthropogenic (wastewater effluent), seabird-derived (guano), and mineral nutrient (inorganic N and P) enrichment sources, in combination with a two-week heat-stress treatment, on the metabolism of two corals in Hawai’i: Montipora capitata and Porites compressa. At ambient temperatures, enrichment affected the species differently: P. compressa showed no response to enrichment, whereas M. capitata exhibited a 26–31% increase in primary production under guano enrichment, with no changes in respiration. Heating depressed M. capitata primary production by 48% and 66% in both control and inorganic-enriched treatments, respectively. However, no comparable thermal stress response was detected in effluent- and guano-enriched corals, suggesting that biotically-derived nutrients ameliorated thermal stress. Post-heating, M. capitata showed no residual effects of prior thermal stress: within each enrichment treatment, metabolic rates were similar between prior-temperature treatments. In contrast, P. compressa was highly sensitive to heat across all enrichment treatments, exhibiting 90-150% reductions in primary production and respiration that persisted weeks after heating ended (3-39% below ambient). Enrichment did not facilitate P. compressa thermal recovery and instead corresponded with dampened productivity relative to controls, both during and after heating. By directly comparing these enrichment sources in a controlled mesocosm study for the first time, this work reveals divergent coral responses that highlight the importance of distinguishing among nutrient sources when evaluating local drivers of coral resilience.

Nutrient availability drives community structure and ecosystem processes, especially in tropical lagoons that are typically oligotrophic but often receive allochthonous inputs from land. Terrestrially derived nutrients are introduced to tropical lagoons by surface runoff and submarine groundwater discharge, which are influenced by seasonal precipitation. However, terrigenous inputs presumably diminish along the onshore–offshore gradients within lagoons. We characterized nutrient availability in the lagoons of a tropical high island, Moorea, French Polynesia, using spatially distributed measurements of nitrogen content in the tissues of a widespread macroalga during the rainy season over 4 yr. We used synoptic water column sampling to identify associations among macroalgal nutrient content and the composition of inorganic macronutrients, dissolved organic matter, and microbial communities. We paired these data with quantifications of land use in nearby watersheds to uncover links between terrestrial factors, aquatic chemistry, and microbial communities. Algal N content was highest near shore and near large, human‐impacted watersheds, and lower at offshore sites. Sites with high algal N had water columns with high nitrite + nitrate, silicate, and increased humic organic matter (based on a fluorescence Humification Index), especially following rain. Microbial communities were differentiated among nearshore habitats and covaried with algal N and water chemistry, supporting the hypothesis that terrigenous nutrient enrichment shapes microbial dynamics in otherwise oligotrophic tropical lagoons. This study reveals that land–sea connections create nutrient subsidies that are important for lagoon biogeochemistry and microbiology, indicating that future changes in land use or precipitation will modify ecosystem processes in tropical lagoons.

Nutrient availability drives community structure and ecosystem processes, especially in tropical lagoons that are typically oligotrophic but often receive allochthonous inputs from land. Terrestrially-derived nutrients are introduced to tropical lagoons by surface runoff and submarine groundwater discharge, which are influenced by seasonal precipitation. Lagoon habitats are distributed along an onshore-offshore gradient; terrigenous inputs presumably diminish along the same continuum. We characterized nutrient enrichment in the lagoons of a tropical high island, Moorea, French Polynesia, using spatially distributed measurements of nitrogen content in the tissues of a widespread macroalga during the rainy season over four years. We used synoptic water column sampling to identify associations among macroalgal nutrient content and the composition of inorganic macronutrients, dissolved organic matter, and microbial communities. We paired these data with quantifications of land use in nearby watersheds to uncover links between terrestrial factors, aquatic chemistry, and microbial communities. Algal N content was highest near shore and near large, human-impacted watersheds, and lower at offshore sites. Sites with high algal N had water columns with high nitrite + nitrate, silicate, and increased humic organic matter (based on a fluorescence humification index), especially following rain. Microbial communities were differentiated among nearshore habitats and covaried with algal N and water chemistry, supporting the hypothesis that terrigenous nutrient enrichment shapes microbial dynamics in otherwise oligotrophic tropical lagoons. This study reveals that land-sea connections create nutrient subsidies that are important for lagoon biogeochemistry and microbiology, indicating that changes in land use or precipitation will modify ecosystem processes in tropical lagoons.

Coral reefs are highly productive ecosystems where bacterioplankton play a critical role in recycling dissolved compounds, enabling corals to thrive in oligotrophic waters. Reefs worldwide exhibit trends of declining coral cover with concomitant increases in macroalgae. This project seeks to understand how these trends may alter microbial carbon and nutrient recycling supporting the resilience of reefs to climate change. Decadal data from the Moorea Coral Reef Long Term Ecological Research program (MCR LTER) show that reefs have suffered significant structural damages from past cyclonic events, ongoing anthropogenic impacts and predator outbreaks (Taramea or Crown-of-thorn starfish Acanthaster planci), resulting in phase shifts from coral to macroalgal dominance. Previous research suggests that phase shifts reduce microbial diversity, increase heterotrophic bacteria and disrupt bacterioplankton recycling, leading to inefficient productivity and further coral decline. Mesocosm experiments simulated coral-dominated, algae-dominated, and post-disturbance reefs (A. planci outbreak) to assess the effects of benthic cover on compositional dynamics of microbial communities and dissolved organic matter. Organic matter (fDOM and DOC) quantification was done via fluorescence spectroscopy and catalytic oxidation, while microbial community analysis was done using flow cytometry with amplicon next generation DNA sequencing. The results of this project will enhance our understanding of the interactions between bacterioplankton communities and benthic species, with implications for carbon fixation and remineralization processes in the oligotrophic ecosystems of the South Pacific. Additionally, findings from this study will provide a valuable baseline for assessing the ecological status of locally managed lagoons, supporting parallel research efforts in remote regions of Tahiti.

Dissolved organic matter (DOM) comprises diverse compounds with variable bioavailability across aquatic ecosystems. The sources and quantities of DOM can influence microbial growth and community structure with effects on biogeochemical processes. To investigate the chemodiversity of labile DOM in tropical reef waters, we tracked microbial utilisation of over 3000 untargeted mass spectrometry ion features exuded from two coral and three algal species. Roughly half of these features clustered into over 500 biologically labile spectral subnetworks annotated to diverse structural superclasses, including benzenoids, lipids, organic acids, heterocyclics and phenylpropanoids, comprising on average one‐third of the ion richness and abundance within each chemical class. Distinct subsets of these labile compounds were exuded by algae and corals during the day and night, driving differential microbial growth and substrate utilisation. This study expands the chemical diversity of labile marine DOM with implications for carbon cycling in coastal environments.

In this era of rapid global change, factors influencing the stability of ecosystems and their functions have come into the spotlight. For decades the relationship between stability and complexity has been investigated in modeled and empirical systems, yet results remain largely context dependent. To overcome this we leverage a multiscale inventory of fungi and bacteria ranging from single sites along an environmental gradient, to habitats inclusive of land, sea and stream, to an entire watershed. We use networks to assess the relationship between microbiome complexity and robustness and identify fundamental principles of stability. We demonstrate that while some facets of complexity are positively associated with robustness, others are not. Beyond positive biodiversity x robustness relationships we find that the number of “gatekeeper” species or those that are highly connected and central within their networks, and the proportion of predicted negative interactions are universal indicators of robust microbiomes. With the potential promise of microbiome engineering to address global challenges ranging from human to ecosystem health we identify properties of microbiomes for future experimental studies that may enhance their stability. We emphasize that features beyond biodiversity and additional characteristics beyond stability such as adaptability should be considered in these efforts.

High molecular weight (HMW; >1 kDa) carbohydrates are a major component of dissolved organic matter (DOM) released by benthic primary producers. Despite shifts from coral to algae dominance on many reefs, little is known about the effects of exuded carbohydrates on bacterioplankton communities in reef waters. We compared the monosaccharide composition of HMW carbohydrates exuded by hard corals and brown macroalgae and investigated the response of the bacterioplankton community of an algae-dominated Caribbean reef to the respective HMW fractions. HMW coral exudates were compositionally distinct from the ambient, algae-dominated reef waters and similar to coral mucus (high in arabinose). They further selected for opportunistic bacterioplankton taxa commonly associated with coral stress (i.e., Rhodobacteraceae , Phycisphaeraceae , Vibrionaceae , and Flavobacteriales ) and significantly increased the predicted energy-, amino acid-, and carbohydrate-metabolism by 28%, 44%, and 111%, respectively. In contrast, HMW carbohydrates exuded by algae were similar to those in algae tissue extracts and reef water (high in fucose) and did not significantly alter the composition and predicted metabolism of the bacterioplankton community. These results confirm earlier findings of coral exudates supporting efficient trophic transfer, while algae exudates may have stimulated microbial respiration instead of biomass production, thereby supporting the microbialization of reefs. In contrast to previous studies, HMW coral and not algal exudates selected for opportunistic microbes, suggesting that a shift in the prevalent DOM composition and not the exudate type (i.e., coral vs algae) per se , may induce the rise of opportunistic microbial taxa. IMPORTANCE: Dissolved organic matter (DOM) released by benthic primary producers fuels coral reef food webs. Anthropogenic stressors cause shifts from coral to algae dominance on many reefs, and resulting alterations in the DOM pool can promote opportunistic microbes and potential coral pathogens in reef water. To better understand these DOM-induced effects on bacterioplankton communities, we compared the carbohydrate composition of coral- and macroalgae-DOM and analyzed the response of bacterioplankton from an algae-dominated reef to these DOM types. In line with the proposed microbialization of reefs, coral-DOM was efficiently utilized, promoting energy transfer to higher trophic levels, whereas macroalgae-DOM likely stimulated microbial respiration over biomass production. Contrary to earlier findings, coral- and not algal-DOM selected for opportunistic microbial taxa, indicating that a change in the prevalent DOM composition, and not DOM type, may promote the rise of opportunistic microbes. Presented results may also apply to other coastal marine ecosystems undergoing benthic community shifts.

Coral reefs are among the most sensitive ecosystems affected by ocean warming and acidification, and are predicted to collapse over the next few decades. Reefs are predicted to shift from net accreting calcifier-dominated systems with exceptionally high biodiversity to net eroding algal-dominated systems with dramatically reduced biodiversity. Here, we present a two-year experimental study examining the responses of entire mesocosm coral reef communities to warming (+2 °C), acidification (−0.2 pH units), and combined future ocean (+2 °C, −0.2 pH) treatments. Contrary to modeled projections, we show that under future ocean conditions, these communities shift structure and composition yet persist as novel calcifying ecosystems with high biodiversity. Our results suggest that if climate change is limited to Paris Climate Agreement targets, coral reefs could persist in an altered state rather than collapse.