Benthic organisms are the architectural framework supporting coral reef ecosystems, but their community composition has recently shifted on many reefs. Little is known about the metabolites released from these benthic organisms and how compositional shifts may influence other reef life, including prolific microorganisms. To investigate the metabolite composition of benthic exudates and their ecological significance for reef microbial communities, we harvested exudates from six species of Caribbean benthic organisms including stony corals, octocorals, and an invasive encrusting alga, and subjected these exudates to untargeted and targeted metabolomics approaches using liquid chromatography-mass spectrometry. Incubations with reef seawater microorganisms were conducted to monitor changes in microbial abundances and community composition using 16 S rRNA gene sequencing in relation to exudate source and three specific metabolites. Exudates were enriched in amino acids, nucleosides, vitamins, and indole-based metabolites, showing that benthic organisms contribute labile organic matter to reefs. Furthermore, exudate compositions were species-specific, and riboflavin and pantothenic acid emerged as significant coral-produced metabolites, while caffeine emerged as a significant invasive algal-produced metabolite. Microbial abundances and individual microbial taxa responded differently to exudates from stony corals and octocorals, demonstrating that exudate mixtures released from different coral species select for specific bacteria. In contrast, microbial communities did not respond to individual additions of riboflavin, pantothenic acid, or caffeine. This work indicates that recent shifts in benthic organisms alter exudate composition and likely impact microbial communities on coral reefs.
Extracellular Reef Metabolites Across the Protected Jardines de la Reina, Cuba Reef System
Coral reef ecosystems are incredibly diverse marine biomes that rely on nutrient cycling by microorganisms to sustain high productivity in generally oligotrophic regions of the ocean. Understanding the composition of extracellular reef metabolites in seawater, the small organic molecules that serve as the currency for microorganisms, may provide insight into benthic-pelagic coupling as well as the complexity of nutrient cycling in coral reef ecosystems. Jardines de la Reina (JR), Cuba is an ideal environment to examine extracellular metabolites across protected and high-quality reefs. Here, we used liquid chromatography mass spectrometry (LC-MS) to quantify specific known metabolites of interest (targeted metabolomics approach) and to survey trends in metabolite feature composition (untargeted metabolomics approach) from surface and reef depth (6 – 14 m) seawater overlying nine forereef sites in JR. We found that untargeted metabolite feature composition was surprisingly similar between reef depth and surface seawater, corresponding with other biogeochemical and physicochemical measurements and suggesting that environmental conditions were largely homogenous across forereefs within JR. Additionally, we quantified 32 of 53 detected metabolites using the targeted approach, including amino acids, nucleosides, vitamins, and other metabolic intermediates. Two of the quantified metabolites, riboflavin and xanthosine, displayed interesting trends by depth. Riboflavin concentrations were higher in reef depth compared to surface seawater, suggesting that riboflavin may be produced by reef organisms at depth and degraded in the surface through photochemical oxidation. Xanthosine concentrations were significantly higher in surface reef seawater. 5′-methylthioadenosine (MTA) concentrations increased significantly within the central region of the archipelago, displaying biogeographic patterns that warrant further investigation. Here we lay the groundwork for future investigations of variations in metabolite composition across reefs, sources and sinks of reef metabolites, and changes in metabolites over environmental, temporal, and reef health gradients.
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- Award ID(s):
- 1736288
- NSF-PAR ID:
- 10313574
- Date Published:
- Journal Name:
- Frontiers in Marine Science
- Volume:
- 7
- ISSN:
- 2296-7745
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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Abstract Coral reef community composition and ecosystem function may change in response to anthropogenic ocean acidification. However, the magnitude of acidification on reefs will be modified by natural spatial and temporal variability in seawater CO2chemistry. Consequently, it is necessary to quantify the ecological, biogeochemical, and physical drivers of this natural variability before making robust predictions of future acidification on reefs. In this study, we measured temporal and spatial physiochemical variability on a reef flat in Kāne‘ohe Bay, O‘ahu, Hawai‘i, using autonomous sensors at sites with contrasting benthic communities and by sampling surface seawater CO2chemistry across the reef flat at different times of the day during June and November. Mean and diurnal temporal variability of seawater CO2chemistry was more strongly influenced by depth gradients (~ 0.5–10 m) on the reef rather than benthic community composition. Spatial CO2chemistry gradients across the reef flat reflected the cumulative influence from benthic metabolism, bathymetry, and hydrodynamics. Based on graphical assessment of total alkalinity–dissolved inorganic carbon data, reef metabolism in November was dominated by organic carbon cycling over inorganic carbon cycling, while these processes were closely balanced in June. Overall, this study highlights the strong influence of depth on reef seawater CO2chemistry variability through its effects on benthic biomass to seawater volume ratio, seawater flow rates, and residence time. Thus, the natural complexity of ecosystems where a combination of ecological and physical factors influence reef chemistry must be considered when predicting ecosystem biogeochemical responses to future anthropogenic changes in seawater CO2chemistry.
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Seawater microorganisms play an important role in coral reef ecosystem functioning and can be influenced by biological, chemical, and physical features of reefs. As coral reefs continue to respond to environmental changes, the reef seawater microbiome has been proposed as a conservation tool for monitoring perturbations. However, the spatial variability of reef seawater microbial communities is not well studied, limiting our ability to make generalizable inferences across reefs. In order to better understand how microorganisms are distributed at multiple spatial scales, we examined seawater microbial communities in Florida Reef Tract and US Virgin Islands reef systems using a nested sampling design. On 3 reefs per reef system, we sampled seawater at regular spatial intervals close to the benthos. We assessed the microbial community composition of these waters using ribosomal RNA gene amplicon sequencing. Our analysis revealed that reef water microbial communities varied as a function of reef system and individual reefs, but communities did not differ within reefs and were not significantly influenced by benthic composition. For the reef system and inter-reef differences, abundant microbial taxa were found to be potentially useful indicators of environmental difference due to their high prevalence and variance. We further examined reef water microbial biogeography on a global scale using a secondary analysis of 5 studies, which revealed that microbial communities were more distinct with increasing geographic distance. These results suggest that biogeography is a distinguishing feature for reef water microbiomes, and that development of monitoring criteria may necessitate regionally specific sampling and analyses.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmars.2020.582161
