Microbial transformation of distinct exogenous substrates into analogous composition of recalcitrant dissolved organic matter

Abstract

Summary Oceanic dissolved organic matter (DOM) comprises a complex molecular mixture which is typically refractory and homogenous in the deep layers of the ocean. Though the refractory nature of deep‐sea DOM is increasingly attributed to microbial metabolism, it remains unexplored whether ubiquitous microbial metabolism of distinct carbon substrates could lead to similar molecular composition of refractory DOM. Here, we conducted microbial incubation experiments using four typically bioavailable substrates (L‐alanine, trehalose, sediment DOM extract, and diatom lysate) to investigate how exogenous substrates are transformed by a natural microbial assemblage. The results showed that although each‐substrate‐amendment induced different changes in the initial microbial assemblage and the amended substrates were almost depleted after 90 days of dark incubation, the bacterial community compositions became similar in all incubations on day 90. Correspondingly, revealed by ultra‐high resolution mass spectrometry, molecular composition of DOM in all incubations became compositionally consistent with recalcitrant DOM and similar toward that of DOM from the deep‐sea. These results indicate that while the composition of natural microbial communities can shift with substrate exposures, long‐term microbial transformation of distinct substrates can ultimately lead to a similar refractory DOM composition. These findings provide an explanation for the homogeneous and refractory features of deep‐sea DOM.

Experimental Insight into the Enigmatic Persistence of Marine Refractory Dissolved Organic Matter

“…More specifically, the bacterial abundance increased in the deep-sea control and PPL- and C18-DOM incubations and lasted over the 180-day period (Figure f), though the DOC concentration was insignificantly decreased in the controls and was only slightly decreased in the PPL- and C18-DOM-amended incubations during the period of days 30–180 (Figure S4c). This could also be explained as heterotrophic utilization of semi-labile and semi-recalcitrant DOM by some microbial specialists, − considering that bacterial succession might take longer than 180 days …”

Increased microbial and substrate complexity result in higher molecular diversity of the dissolved organic matter pool

“…Recently a study has revealed that natural microorganisms can utilize and transform four different substrates with different complexities (L-alanine, trehalose, sediment DOM extract, and diatom lysate) into a DOM pool with a similar composition (Lian et al 2021). However, in that study the large background DOM signal hindered further identification of newly produced organic molecules under different substrate conditions.…”

Epiphytic Bacteria Are Essential for the Production and Transformation of Algae-Derived Carboxyl-Rich Alicyclic Molecule (CRAM)-like DOM

“…Previous studies have shown that axenic cultures of multiple species of algae contribute to detectable humic-like DOM in the ocean ( 21 ), while others indicated that aggregation of recalcitrant DOM results from microbial processing (mainly bacteria) of planktonic-precursors ( 22 ). Incubation experiments have also demonstrated that heterotrophic bacteria in the marine environment can convert glucose, glutamic acid, oligosaccharides, and algae extracts into highly diverse recalcitrant components ( 16 , 23 , 24 ). These exometabolites directly released by bacteria upon utilization of labile substrates ought to have intrinsic properties rendering them resistant to decomposition and therefore allowing them to remain recalcitrant for a long time ( 16 , 21 , 25 – 27 ).…”