Dissolved Organic Carbon in Organic-Rich Aquatic Ecosystems: Biodegradability and an Assessment of the Priming Effect

Rivers deliver approximately 260 Tg of dissolved organic carbon (DOC) to the ocean annually, yet there is little evidence of terrigenous DOC (tDOC) in the ocean. While tDOC was historically believed to be stable and resistant to microbial degradation, it has recently been shown that freshwater systems mineralize more tDOC than originally thought. Biodegradability of DOC is an overriding control on ecosystem respiration, regulating how much organic carbon is remineralized as CO2 or exported downstream, however, the processes controlling DOC degradation are not well understood. The priming effect is a possible mechanism by which inputs of biolabile DOC enhance the bioavailability of stable DOC components in aquatic systems, resulting in higher rates of microbial remineralization. Here we investigate microbial degradation of DOC by conducting bioincubation experiments and assessing a variety of biogeochemical controls on DOC biolability, including the priming effect, nutrient availability, seasonality, and chemical composition. The role of priming and nutrient availability was assessed through the inclusion of bioincubation treatments amended with nutrients and a variety of simple biolabile organic carbon substrates. Ultrahigh resolution mass spectrometry allowed us to characterize the molecular composition of dissolved organic matter (DOM) samples and understand how chemical composition may act as a driver of DOM biodegradability. This study was first conducted on blackwater systems in Florida, where we collected blackwater river samples and made leachates from plant litter that largely contributes to the terrestrial input of organic matter in these systems. Blackwaters consist of a diverse mixture of organic substances and are ideal study sites for assessing biodegradability of DOC and priming as they are rich in organic matter (i.e. high DOC concentrations), dominated by DOM that is highly aromatic in nature, and are historically believed to be a stable DOM pool. During the bioincubation experiments, blackwaters lost 6.10 ± 3.85% DOC within one month, while leachates lost 38.10 ± 16.74% DOC. There were no significant differences between DOC remineralization in control and ‘primed’ treatments, indicating that priming is not an important factor in the biodegradation of DOC in blackwater ecosystems. However, the proportion of biodegradable DOC (BDOC) and DOM composition were significantly correlated, mostly driven by the contribution of aliphatic compounds (H/C ≥ 1.5, O/C < 0.9) that were abundant (9.3 ± 5.2%) in leachate DOM. The molecular signature of biodegraded leachate DOM resembled that of stable blackwater DOM, indicating that bioavailable DOM components leached from plant litter are rapidly utilized and stable DOM is exported downstream. Further, we conducted this study on permafrost-influenced streams in the Yukon Flats of Interior Alaska, a region underlain by discontinuous permafrost that is experiencing rapidly warming temperatures, permafrost thaw, and associated changes in hydrology and vegetation, all which affect the biodegradability and fate of DOC. Permafrost-influenced streams may also be sites of ‘priming effects’ as biolabile, ancient permafrost DOC mixes with relatively modern, stable stream DOC. To determine the vulnerability of DOC in this region to microbial degradation, we conducted 28-day bioincubation experiments utilizing a suite of stream samples and leachates made from fresh ground vegetation and several soil layers collected at different depths, including permafrost. Microbial utilization of stream DOC ranged from 4 to 11% in spring and differences were likely influenced by site drainage characteristics. Leachate DOC followed a continuum of biodegradability, losing from 9% (mineral soil-derived) to as much as 66% (vegetation-derived) DOC. Nutrient availability rather than priming controlled DOC remineralization, especially for fall stream samples and mineral soil leachates. Seasonally, it appears that DOC biodegradability and aromaticity decrease into fall. The molecular composition of DOM determined by ultra-high resolution mass spectrometry was significantly correlated to DOC biodegradability, particularly the contribution of aliphatic compounds. Stream microbial communities utilized 50-56% of aliphatic compounds in permafrost-derived DOM within 28 days. We also found evidence for selective preservation of aromatic DOM compounds with depth in soil horizons. Our findings imply that future climate-driven changes (e.g. temperature, nutrient supply, and vegetation) in discontinuous permafrost regions may cause the release of biolabile DOM that is rapidly respired, resulting in a positive feedback with climate change.

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