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

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.

Meta-transcriptomic comparison of two sponge holobionts feeding on coral- and macroalgal-dissolved organic matter

“…By suppressing glycolysis, TIGAR causes the accumulation of glucose 6-phosphate that is then diverted into the pentose phosphate (PP) pathway to generate nucleotides, NADPH, and antioxidants, which help repair DNA, reduce reactive oxygen species and support rapid cell proliferation [ 91 , 92 ]. While macroalgae release DOM composed of labile carbohydrates, which can be shunted directly in the PP pathway [ 17 ], coral-DOM is usually richer in proteins and fatty acids [ 15 , 93 ]. Therefore, the upregulation of a mechanism that activates the PP pathway may be required to assist rapid cell proliferation in sponges feeding on coral-DOM.…”

“…In the past twenty years, considerable changes in benthic communities, such as a shift from coral to algal dominance, have occurred on many coral reefs as a consequence of climatic events in combination with direct anthropogenic disturbances [ 12 – 14 ]. Benthic algae, including turf algae and macroalgae, are found to release higher amounts of bioavailable DOM than corals [ 15 , 16 ], which results in higher growth rates of ambient bacterioplankton, including the growth of pathogenic bacteria [ 16 – 19 ]. Recently, differential processing of naturally sourced coral- and macroalgal-DOM has been observed also in sponges, showing that macroalgal-DOM is generally more bioavailable to the sponge holobiont than coral-DOM [ 20 , 21 ].…”

Cultivation of different seaweed species and seasonal changes cause divergence of the microbial community in coastal seawaters

“…Furthermore, organic matter released by algae can be stored, respired as DOC, or put into growth together with other nutrients such as phosphate and nitrogen, then utilized directly by microbes ( Anderson and Ducklow, 2001 ; Jiao et al, 2010 ). DOC released by seaweed is composed of free amino acids, sugars, and organic acids ( Thornton, 2014 ; Wegley Kelly et al, 2022 ). Among these organic substances, the algal polysaccharides are potential sources of carbon and energy for various marine bacteria ( Goecke et al, 2010 ; Hehemann et al, 2012 ).…”

“…In addition, the patterns in multivariate exo-metabolites featured variation among different seaweeds. The molecular structures of these compounds are one factor affecting the community of microorganisms that metabolize the compounds ( Wegley Kelly et al, 2022 ). Thus, we suggest that the vast metabolic diversity of natural compounds produced by seaweed may provide a basis for selectively promoting, inhibiting, and recruiting specific microbes to enable the shaping of microbial communities tailored to the seawater properties.…”

Mass Difference Matching Unfolds Hidden Molecular Structures of Dissolved Organic Matter

“…Complex mixtures are key study objects in environmental and industrial applications, but their analysis remains challenging. − One of the most complex mixtures in natural ecosystems is dissolved organic matter (DOM). , DOM is a central intermediate of ecosystem metabolism and mirrors molecular imprints of interactions with its abiotic and biotic environment, − which form the basis for processes such as carbon sequestration and nutrient recycling. , Despite significant advances in ultrahigh-resolution mass spectrometry (FTMS) , and nuclear magnetic resonance spectroscopy, scientists still struggle to decode this information on the molecular level, − and novel approaches to identify distinct structures are required to translate molecular-level information into improved process understanding.…”