Release of ecologically relevant metabolites by the cyanobacterium Synechococcus elongatus CCMP 1631

Abstract

Photoautotrophic plankton in the surface ocean release organic compounds that fuel secondary production by heterotrophic bacteria. Here we show that an abundant marine cyanobacterium, Synechococcus elongatus, contributes a variety of nitrogen-rich and sulfur-containing compounds to dissolved organic matter. A combination of targeted and untargeted metabolomics and genomic tools was used to characterize the intracellular and extracellular metabolites of S. elongatus. Aromatic compounds such as 4-hydroxybenzoic acid and phenylalanine, as well as nucleosides (e.g., thymidine, 5'-methylthioadenosine, xanthosine), the organosulfur compound 3-mercaptopropionate, and the plant auxin indole 3-acetic acid, were released by S. elongatus at multiple time points during its growth. Further, the amino acid kynurenine was found to accumulate in the media even though it was not present in the predicted metabolome of S. elongatus. This indicates that some metabolites, including those not predicted by an organism's genome, are likely excreted into the environment as waste; however, these molecules may have broader ecological relevance if they are labile to nearby microbes. The compounds described herein provide excellent targets for quantitative analysis in field settings to assess the source and lability of dissolved organic matter in situ.

Dynamic metabolic exchange governs a marine algal-bacterial interaction

“…Previously, tryptophan was identified as a key metabolite in the interaction between a diatom and a Roseobacter (Amin et al, 2015). The use of both targeted and untargeted metabolomics in the lab can greatly aid in identifying metabolites with ecological relevance (Fiore et al, 2015; Johnson et al, 2016; Durham et al, 2015; Amin et al, 2015). As revealed in the current study, when microorganisms are in close proximity, molecules can be produced and rapidly consumed and thus remain undetectable.…”

Deciphering ocean carbon in a changing world

“…For example, monomeric amino acids and sugars have concentrations below one billionth of a gram per liter, which is at or below the limits of quantification in marine waters (36,37). However, detecting low-concentration high-flux compounds has recently become more tractable with methodological advances in chemistry [e.g., better separation methodologies, sensitivity, accuracy, and resolving power (5,38,39)], biology [e.g., deducing key substrates from transcriptome analysis (28,29,40)], and cyberinfrastructure [e.g., determining patterns of DOM−bacterial interaction networks (41)]. The complementarity of these research fields is key to identifying this massive yet all but invisible flux in the ocean's active carbon cycle (Fig.…”

“…Many marine phytoplankton with critical roles in global carbon fixation have lost biosynthetic pathways for N-, P-, and S-rich vitamins such as B 1 and B 12 (61) and must scavenge them from the DOM pool. Genomic data have been ideal for learning which marine microbes depend on the DOM pool for energetically expensive biomolecules, whereas metabolomics advances have detected dilute components of DOM that were previously not measurable (39,46).…”

“…New categories of nonpredatory microbial alliances that release organic compounds into seawater are also being recognized. These include molecules in microbial cytosols and exudates (39,68) that serve as substrates, signaling molecules, and allelochemicals to neighboring microbes (69,70). Genes able to mediate microbial interactions have also been uncovered (71,72), including a high prevalence of virulence gene homologs in marine bacteria and archaea that could facilitate direct contact with eukaryotic plankton (73).…”

“…Correspondingly, nontargeted workflows are helping us to discover new molecules we didn't know to look for (33,39,70,105,135). Newly developed informatics approaches are supporting data mining across multiple studies and systems (136,137) (see Box 1).…”