Rapid microbial diversification of dissolved organic matter in oceanic surface waters leads to carbon sequestration

Abstract

The pool of dissolved organic matter (DOM) in the deep ocean represents one of the largest carbon sinks on the planet. In recent years, studies have shown that most of this pool is recalcitrant, because individual compounds are present at low concentrations and because certain compounds seem resistant to microbial degradation. The formation of the diverse and recalcitrant deep ocean DOM pool has been attributed to repeated and successive processing of DOM by microorganisms over time scales of weeks to years. Little is known however, about the transformation and cycling that labile DOM undergoes in the first hours upon its release from phytoplankton. Here we provide direct experimental evidence showing that within hours of labile DOM release, its breakdown and recombination with ambient DOM leads to the formation of a diverse array of new molecules in oligotrophic North Atlantic surface waters. Furthermore, our results reveal a preferential breakdown of N and P containing molecules versus those containing only carbon. Hence, we show the preferential breakdown and molecular diversification are the crucial first steps in the eventual formation of carbon rich DOM that is resistant to microbial remineralization.

Figure 1

Changes in particulate and dissolved organic matter over time in oligotrophic surface waters (A) Organic matter concentrations in incubations amended with ¹³C-DOM (error bars are SD n = 3). (B) ¹³CO₂ production from ¹³C-DOM (error bars are SD, n = 3) and number of DO¹³C molecules (C) summed normalized intensities of all DO¹³C molecules measured by the FT-ICR-MS and their average labeling percentage at each time point. The grey area denotes the night/dark period during the incubation. Note that the error bars are smaller than the bullets in many cases. POC = Particulate Organic Carbon, DOC = Dissolved Organic Carbon, PON = Particulate Organic Nitrogen, DON = Dissolved Organic Nitrogen.

Figure 2

Rapid breakdown and transformation of labile ¹³C-DOM molecules in oligotrophic surface waters. Outer ring: Heatmap of the normalized FT-ICR-MS intensities of all detected ¹³C labelled molecules during the incubation. ¹³C labelled molecules are grouped based on their presence at all, three, two or one time point. Inner ring: Heteroatom composition of each molecular formula; colours represent molecular formulas only containing CHO (white), containing nitrogen (green), phosphorus (magenta) or nitrogen and phosphorus (green and magenta). Centre panel: Relative abundance of molecules based on heteroatom composition, where the size is representative of the total number of molecules present at all, three, two or one time point. See Sup. Table 1 for the molecular formulas of the 106 compounds. Note the axis break in the linear color scale of the normalized intensities.