Dissolved organic matter composition and temperature determine organic carbon utilization in the deep ocean

Dissolved organic matter (DOM) represents the largest and chemically diverse reservoir of reduced carbon (~630 Gt C) in the ocean. However, the overwhelming majority is considered biologically recalcitrant (RDOC), resisting rapid biological degradation. To date, the “recalcitrance” of organic compounds in the deep sea is attributed to three main limitations: (I) Deep-sea organic matter may be inaccessible to microorganisms due to its extremely low concentrations of individual components (limitation hypothesis). (II) The molecular structure of deep-sea DOM could be inherently resistant to microbial utilization (recalcitrance hypothesis). (III) The metabolic capabilities of deep-sea microbes might be constrained, e.g., by low temperature and high hydrostatic pressure, limiting their ability to process available organic matter. In addition, the impact of global warming-induced temperature increases in the bathypelagic zone and their consequent effects on deep-sea DOM dynamics remain poorly understood. Here, we show results from a long-term incubation experiment (222 days) with Pacific deep water bacterioplankton, from the Humboldt Current System, exposed to two sources of high molecular weight dissolved organic matter (HMW-DOM, 1-30 kDa), obtained from a) the surface and b) the deep sea (1500 m), along with a detailed characterization of micro(biological) and chemical parameters, at in situ (+2.5°C) and elevated temperature (+6.5°C). The addition of the two DOM sources to deep sea bacterioplankton stimulated bacterial activity (cell abundance, biomass production, and extracellular enzyme activity). However, amendments with deep sea DOM - characterized by more similar carbohydrate and amino acid composition than the surface (Euclidean distance) - resulted in higher bacterial biomass production. This effect increased up to 4-fold under elevated temperature (+6.5°C), while DOC and TOC decreased by ~10 µM C by the end of the experiment. Biochemical characterization of DOM components (i.e., dissolved hydrolyzable carbohydrates and amino acids), collectively accounting for ~6% of DOC, showed a selective consumption of galacturonic acid and glucuronic acid, contributing ~2% of total sugars, and alanine and serine at the end of the experiment (decrease in mol% and nM). These findings suggest that i) increasing the concentration of HMW-DOM components stimulates bacterioplankton activity, ii) these organic components are generally accessible to deep-sea microbes, and iii) the bathypelagic microbiome is capable of metabolizing HMW-DOM. Furthermore, the several-fold increase in bacterial activity observed under a simulated warming scenario (+4.0°C) indicates that climate change-induced warming of the bathypelagic zone could enhance deep-sea DOM utilization. This, in turn, has the potential to alter marine biogeochemical cycles, introducing feedback loops that remain poorly understood.