Coral thermal stress and bleaching enrich and restructure reef microbial communities via altered organic matter exudation.

Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events

Lipidomics of Environmental Microbial Communities. I: Visualization of Component Distributions Using Untargeted Analysis of High-Resolution Mass Spectrometry Data

<jats:p>Lipids, as one of the main building blocks of cells, can provide valuable information on microorganisms in the environment. Traditionally, gas or liquid chromatography coupled to mass spectrometry (MS) has been used to analyze environmental lipids. The resulting spectra were then processed through individual peak identification and comparison with previously published mass spectra. Here, we present an untargeted analysis of MS<jats:sup>1</jats:sup> spectral data generated by ultra-high-pressure liquid chromatography coupled with high-resolution mass spectrometry of environmental microbial communities. Rather than attempting to relate each mass spectrum to a specific compound, we have treated each mass spectrum as a component, which can be clustered together with other components based on similarity in their abundance depth profiles through the water column. We present this untargeted data visualization method on lipids of suspended particles from the water column of the Black Sea, which included >14,000 components. These components form clusters that correspond with distinct microbial communities driven by the highly stratified water column. The clusters include both known and unknown compounds, predominantly lipids, demonstrating the value of this rapid approach to visualize component distributions and identify novel lipid biomarkers.</jats:p&gt

DataSheet_2_Sponges on shifting reefs: holobionts show similar molecular and physiological responses to coral versus macroalgal food.xlsx

IntroductionMany coral reefs witness an ongoing coral-to-algae phase shift. Corals and algae release large quantities of (in)organic nutrients daily, of which a large part is utilized by sponges. In turn, sponges are important cyclers of precious resources to other inhabitants on reefs residing in oligotrophic waters. Here, we investigated whether sponge holobionts (i.e., host and prokaryotic symbionts) adapt their physiology to food released by coral- versus macroalgae.MethodsThereto, two sponge species, Plakortis angulospiculatus and Halisarca caerulea (high and low microbial abundance, respectively), were continuously exposed for 12 days to coral and macroalgal exudates in running seawater aquaria. Transcript expression of host and prokaryotic symbionts, changes in prokaryotic community composition, and holobiont physiological responses (i.e., respiratory demand, fluxes of carbon and nitrogen) were investigated after coral- versus macroalgae dominated treatments and compared to a seawater only control treatment.ResultsIn both sponge holobionts differential transcript expression between the coral and macroalgae treatments was very low (DiscussionAfter 12 days of exposure sponges appear to opportunistically feed on different food sources without having to adjust their metabolic pathways or associated prokaryotic communities. This suggests that sponges could be well-adapted to predicted changes in food source availability due to coral-to-algal phase shifts on many coral reefs.</p

Distinguishing the molecular diversity, nutrient content, and energetic potential of exometabolomes produced by macroalgae and reef-building corals.

Metabolites exuded by primary producers comprise a significant fraction of marine dissolved organic matter, a poorly characterized, heterogenous mixture that dictates microbial metabolism and biogeochemical cycling. We present a foundational untargeted molecular analysis of exudates released by coral reef primary producers using liquid chromatography-tandem mass spectrometry to examine compounds produced by two coral species and three types of algae (macroalgae, turfing microalgae, and crustose coralline algae [CCA]) from Moorea, French Polynesia. Of 10,568 distinct ion features recovered from reef and mesocosm waters, 1,667 were exuded by producers; the majority (86%) were organism specific, reflecting a clear divide between coral and algal exometabolomes. These data allowed us to examine two tenets of coral reef ecology at the molecular level. First, stoichiometric analyses show a significantly reduced nominal carbon oxidation state of algal exometabolites than coral exometabolites, illustrating one ecological mechanism by which algal phase shifts engender fundamental changes in the biogeochemistry of reef biomes. Second, coral and algal exometabolomes were differentially enriched in organic macronutrients, revealing a mechanism for reef nutrient-recycling. Coral exometabolomes were enriched in diverse sources of nitrogen and phosphorus, including tyrosine derivatives, oleoyl-taurines, and acyl carnitines. Exometabolites of CCA and turf algae were significantly enriched in nitrogen with distinct signals from polyketide macrolactams and alkaloids, respectively. Macroalgal exometabolomes were dominated by nonnitrogenous compounds, including diverse prenol lipids and steroids. This study provides molecular-level insights into biogeochemical cycling on coral reefs and illustrates how changing benthic cover on reefs influences reef water chemistry with implications for microbial metabolism

DataSheet_1_Sponges on shifting reefs: holobionts show similar molecular and physiological responses to coral versus macroalgal food.xlsx

IntroductionMany coral reefs witness an ongoing coral-to-algae phase shift. Corals and algae release large quantities of (in)organic nutrients daily, of which a large part is utilized by sponges. In turn, sponges are important cyclers of precious resources to other inhabitants on reefs residing in oligotrophic waters. Here, we investigated whether sponge holobionts (i.e., host and prokaryotic symbionts) adapt their physiology to food released by coral- versus macroalgae.MethodsThereto, two sponge species, Plakortis angulospiculatus and Halisarca caerulea (high and low microbial abundance, respectively), were continuously exposed for 12 days to coral and macroalgal exudates in running seawater aquaria. Transcript expression of host and prokaryotic symbionts, changes in prokaryotic community composition, and holobiont physiological responses (i.e., respiratory demand, fluxes of carbon and nitrogen) were investigated after coral- versus macroalgae dominated treatments and compared to a seawater only control treatment.ResultsIn both sponge holobionts differential transcript expression between the coral and macroalgae treatments was very low (DiscussionAfter 12 days of exposure sponges appear to opportunistically feed on different food sources without having to adjust their metabolic pathways or associated prokaryotic communities. This suggests that sponges could be well-adapted to predicted changes in food source availability due to coral-to-algal phase shifts on many coral reefs.</p

DataSheet_3_Sponges on shifting reefs: holobionts show similar molecular and physiological responses to coral versus macroalgal food.pdf

IntroductionMany coral reefs witness an ongoing coral-to-algae phase shift. Corals and algae release large quantities of (in)organic nutrients daily, of which a large part is utilized by sponges. In turn, sponges are important cyclers of precious resources to other inhabitants on reefs residing in oligotrophic waters. Here, we investigated whether sponge holobionts (i.e., host and prokaryotic symbionts) adapt their physiology to food released by coral- versus macroalgae.MethodsThereto, two sponge species, Plakortis angulospiculatus and Halisarca caerulea (high and low microbial abundance, respectively), were continuously exposed for 12 days to coral and macroalgal exudates in running seawater aquaria. Transcript expression of host and prokaryotic symbionts, changes in prokaryotic community composition, and holobiont physiological responses (i.e., respiratory demand, fluxes of carbon and nitrogen) were investigated after coral- versus macroalgae dominated treatments and compared to a seawater only control treatment.ResultsIn both sponge holobionts differential transcript expression between the coral and macroalgae treatments was very low (DiscussionAfter 12 days of exposure sponges appear to opportunistically feed on different food sources without having to adjust their metabolic pathways or associated prokaryotic communities. This suggests that sponges could be well-adapted to predicted changes in food source availability due to coral-to-algal phase shifts on many coral reefs.</p

Coral thermal stress and bleaching enrich and restructure reef microbial communities via altered organic matter exudation

Abstract Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events

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 sequenc- ing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the hol- obiont 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 abun- dances and larger microbial cells. This was consistent with previ- ous 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 metabo- lites 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 sup- ported 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 micro - biome, 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

Small-scale oxygen distribution patterns in a coral reef

One mechanism giving fleshy algae a competitive advantage over corals during reef degradation is algal-induced and microbially-mediated hypoxia (typically less than 69.5 µmol oxygen L−1). During hypoxic conditions oxygen availability becomes insufficient to sustain aerobic respiration in most metazoans. Algae are more tolerant of low oxygen conditions and may outcompete corals weakened by hypoxia. A key question on the ecological importance of this mechanism remains unanswered: How extensive are local hypoxic zones in highly turbulent aquatic environments, continuously flushed by currents and wave surge? To better understand the concert of biological, chemical, and physical factors that determine the abundance and distribution of oxygen in this environment, we combined 3D imagery, flow measurements, macro- and micro-organismal abundance estimates, and experimentally determined biogenic oxygen and carbon fluxes as input values for a 3D bio-physical model. The model was first developed and verified for controlled flume experiments containing coral and algal colonies in direct interaction. We then developed a three-dimensional numerical model of an existing coral reef plot off the coast of Curaçao where oxygen concentrations for comparison were collected in a small-scale grid using fiberoptic oxygen optodes. Oxygen distribution patterns given by the model were a good predictor for in situ concentrations and indicate widespread localized differences exceeding 50 µmol L-1 over distances less than a decimeter. This suggests that small-scale hypoxic zones can persist for an extended period of time in the turbulent environment of a wave- and surge- exposed coral reef. This work highlights how the combination of three-dimensional imagery, biogenic fluxes, and fluid dynamic modeling can provide a powerful tool to illustrate and predict the distribution of analytes (e.g., oxygen or other bioactive substances) in a highly complex system.</p