An official website of the United States government
Scleractinian corals are bathed in a sea of planktonic and particle-associated microorganisms. The metabolic products of corals influence the growth and composition of microorganisms, but interactions between corals and seawater microorganisms are underexplored. We conducted a field-based survey to compare the biomass, diversity, composition, and functional capacity of microorganisms in small-volume seawater samples collected adjacent to five coral species with seawater collected > 1 m away from the reef substrate on the same reefs. Seawater collected close to corals generally harbored copiotrophic-type bacteria and its bacterial and archaeal composition was influenced by coral species as well as the local reef environment. Trends in picoplankton abundances were variable and either increased or decreased away from coral colonies based on coral species and picoplankton functional group. Genes characteristic of surface-attached and potentially virulent microbial lifestyles were enriched in near coral seawater compared to reef seawater. There was a prominent association between the coral Porites astreoides and the coral symbiont Endozoicomonas, suggesting recruitment and/or shedding of these cells into the surrounding seawater. This evidence extends our understanding of potential species-specific and reef site-influenced microbial interactions that occur between corals and microorganisms within this near-coral seawater environment that we propose to call the “coral ecosphere.” Microbial interactions that occur within the coral ecosphere could influence recruitment of coral-associated microorganisms and facilitate the transfer of coral metabolites into the microbial food web, thus fostering reef biogeochemical cycling and a linkage between corals and the water column.
more »
« less
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.
more »
« less
- Award ID(s):
- 1736288
- 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
More Like this
-
-
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
-
Globally, coral reef ecosystems are undergoing significant change related to climate change and anthropogenic activities. Yet, the Cuban archipelago of Jardines de la Reina (JR) has experienced fewer stressors due to its geographical remoteness and high level of conservation. This study examines the surface and benthic reef water microbial communities associated with 32 reef sites along the JR archipelago and explores the relationship between the community composition of reef microorganisms examined using bacterial and archaeal small subunit ribosomal RNA gene (16S rRNA gene) sequencing compared to geographic, conservation/protection level, environmental, physicochemical, and reef benthic and pelagic community features. Reef nutrient concentrations were low and microbial communities dominated by picocyanobacteria and SAR11 and SAR86 clade bacteria, characteristic of an oligotrophic system. Reef water microbial community alpha and beta diversity both varied throughout the archipelago and were strongly related to geography. Three sites in the western archipelago showed unique microbial communities, which may be related to the hydrogeography and influences of the channels linking the Ana Maria gulf with the Caribbean Sea. Overall, this work provides the first extensive description of the reef microbial ecology of the Caribbean’s ‘Crown Jewel’ reef system and a framework to evaluate the influence of ongoing stressors on the reef microorganisms.more » « less
-
Metabolomics is a tool with immense potential for providing insight into the impact of biological processes on the environment. Here, we used metabolomics methods to characterize intracellular metabolites within marine microorganisms during a manipulation experiment that was designed to test the impact of two sources of microbial mortality, protozoan grazing and viral lysis. Intracellular metabolites were analyzed with targeted and untargeted mass spectrometry methods. The treatment with reduced viral mortality showed the largest changes in metabolite concentrations, although there were organic compounds that shifted when the impact of protozoan grazers was reduced. Intracellular concentrations of guanine, phenylalanine, glutamic acid, and ectoine presented significant responses to changes in the source of mortality. Unexpectedly, variability in metabolite concentrations were not accompanied by increases in microbial abundance which indicates that marine microorganisms altered their internal organic carbon stores without changes in biomass or microbial growth. We used Weighted Correlation Network Analysis (WGCNA) to identify correlations between the targeted and untargeted mass spectrometry data. This analysis revealed multiple unknown organic compounds were correlated with compatible solutes, also called osmolytes or chemical chaperones, which emphasizes the dominant role of compatible solutes in marine microorganisms.more » « less
-
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 Mo’orea, 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.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmars.2020.582161
