Marine sequestration of carbon in bacterial metabolites

Abstract

Linking microbial metabolomics and carbon sequestration in the ocean via refractory organic molecules has been hampered by the chemical complexity of dissolved organic matter (DOM). Here, using bioassay experiments and ultra-high resolution metabolic profiling, we demonstrate that marine bacteria rapidly utilize simple organic molecules and produce exometabolites of remarkable molecular and structural diversity. Bacterial DOM is similar in chemical composition and structural complexity to naturally occurring DOM in sea water. An appreciable fraction of bacterial DOM has molecular and structural properties that are consistent with those of refractory molecules in the ocean, indicating a dominant role for bacteria in shaping the refractory nature of marine DOM. The rapid production of chemically complex and persistent molecules from simple biochemicals demonstrates a positive feedback between primary production and refractory DOM formation. It appears that carbon sequestration in diverse and structurally complex dissolved molecules that persist in the environment is largely driven by bacteria.

Inefficient microbial production of refractory dissolved organic matter in the ocean

“…One of the most promising techniques is, albeit its limitations, Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR-MS) 16 . The molecular diversity of microbially formed DOM assessed by this approach is very similar to natural oceanic RDOM 17,18 . A currently unresolved conundrum is the observation that RDOM is apparently produced by microorganisms from labile substrates with far higher efficiency than required to sustain the characteristics of the natural DOM pool 11,12,17 .…”

Formation of Chromophoric Dissolved Organic Matter by Bacterial Degradation of Phytoplankton-Derived Aggregates

“…However, with no terrestrial material in our culture experiments, the humic-like fluorescence has to be a direct product of autochthonous production and microbial transformation. Similar processes occurring in the open-ocean water column would explain the global observations of elevated fluorescence and correlations with AOU in the deep ocean (Chen and Bada, 1992;Yamashita et al, 2007;Yamashita and Tanoue, 2008;Jørgensen et al, 2011;Catalá et al, 2015) that has been linked to the remineralization of organic matter and formation of RDOM (Yamashita et al, 2007;Jiao et al, 2010;Hansell, 2013;Lechtenfeld et al, 2015).…”

“…The structural complexity may arise as a direct result of marine snow formation and microbial processing. Aggregation during particle formation could bring aromatic aldehydes and ketones in close proximity with hydroxylated benzoic acid derivatives through the microbial reprocessing into more complex molecules such as RDOM (Lechtenfeld et al, 2015). The presence of these molecules in the same moiety could facilitate charge transfer interactions between electron acceptors and donors, which has been suggested for lignin derivatives (Del Vecchio and Blough, 2004;Baluha et al, 2013;Sharpless and Blough, 2014).…”

“…Sinking aggregates (or marine snow) are an amalgam of intact phytoplankton cells, detritus, fecal pellets, silica and/or carbonate frustules (that provide ballast) and transparent exopolymeric material (TEP) (Alldredge and Silver, 1988). These aggregates exhibit a wide variability with respect to chemical composition Lee, 1989, 1993;Minor et al, 2003) and may result in significant export of organic matter to depth (e.g., Hansell et al, 2009;Carlson et al, 2010) and contribution to refractory DOM (RDOM) formation (Lechtenfeld et al, 2015).…”

Microbially-Mediated Transformations of Estuarine Dissolved Organic Matter

“…Characterizing DOM degradation remains challenging, however, due to the complex nature of DOM, the variety of microbial metabolic pathways, and the various environmental conditions that regulate bacterial metabolism (Eichinger et al, 2011). Despite these challenges, much has been learned by tracking changes in DOC concentration and DOM composition during incubation experiments, including the variation in biomineralization rates as a function of DOM source (e.g., Moran and Zepp, 1997;Obernosterer and Benner, 2004), the relationship of microbial activity to the production of labile (e.g., Kawasaki and Benner, 2006) and refractory (e.g., Ogawa et al, 2001;Jiao et al, 2010;Lechtenfeld et al, 2015) DOM, and how bacterial-derived refractory material compares structurally to refractory DOM in the ocean (e.g., Osterholz et al, 2015). Studies using ultrahigh resolution mass spectrometry have revealed additional molecular-level transformations in DOM as a result of microorganism activity (Kujawinski et al, 2004), including a significant decrease in the molecular diversity of terrigenous DOM (Seidel et al, 2015) and a preferential degradation of oxygen-rich molecules on a time scale of several days (Kim et al, 2006;Medeiros et al, 2015c;Seidel et al, 2015).…”