Abstract
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.
Highlights
Coral reefs j metabolomics j molecular networking capacity of the microbial community in an environment [6]
The molecular structure of these compounds is one factor structuring the community of microorganisms that metabolize them; in turn, this microbial metabolism mediates the composition of dissolved organic matter (DOM)
To collect exudates of benthic primary producers triplicate specimens of five common primary producers from different functional groups were collected and acclimated for several days in water tables: the hermatypic zooxanthellate scleractinian corals Porites lobata and Pocillopora verrucosa, one species of rhodolithic crustose coralline algae (CCA) Hydrolithon reinboldii, the macroalga Dictyota ceylanica, and a typical mixed consortium of benthic turfing algae attached to dead coral rubble (Turf)
Summary
Coral reefs j metabolomics j molecular networking capacity of the microbial community in an environment [6]. This study unveils coral reef DOM by identifying a myriad of specific metabolite classes released into the surrounding waters by reef-building corals and algae, further characterizing their energetic and nutrient content and providing a foundation for linking benthic ecology with microbial processes that influence both the livelihood and demise of coral reefs. Benthic primary producers— corals (via their photosynthetic endosymbionts) and algae— impact the concentrations of oxygen, inorganic carbon, and mineral nutrients in the oceanic waters that bathe the reef platform through photosynthesis, respiration, and calcification [2] These benthic primary producers exude significant amounts of dissolved organic matter (DOM) directly into the surrounding waters (averaging 30% of fixed carbon) [3, 4], establishing the base of a robust microbial food web [5]. Rapid advances in computational tools have been crucial for moving into the realm of dark metabolomics [24], where elemental composition and compound class-level information can be assigned to detected features with tandem fragmentation spectra with increasing confidence [22, 25,26,27]
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