Evidence for key enzymatic controls on metabolism of Arctic river organic matter

Abstract

Permafrost thaw in the Arctic driven by climate change is mobilizing ancient terrigenous organic carbon (OC) into fluvial networks. Understanding the controls on metabolism of this OC is imperative for assessing its role with respect to climate feedbacks. In this study, we examined the effect of inorganic nutrient supply and dissolved organic matter (DOM) composition on aquatic extracellular enzyme activities (EEAs) in waters draining the Kolyma River Basin (Siberia), including permafrost-derived OC. Reducing the phenolic content of the DOM pool resulted in dramatic increases in hydrolase EEAs (e.g., phosphatase activity increased >28-fold) supporting the idea that high concentrations of polyphenolic compounds in DOM (e.g., plant structural tissues) inhibit enzyme synthesis or activity, limiting OC degradation. EEAs were significantly more responsive to inorganic nutrient additions only after phenolic inhibition was experimentally removed. In controlled mixtures of modern OC and thawed permafrost endmember OC sources, respiration rates per unit dissolved OC were 1.3-1.6 times higher in waters containing ancient carbon, suggesting that permafrost-derived OC was more available for microbial mineralization. In addition, waters containing ancient permafrost-derived OC supported elevated phosphatase and glucosidase activities. Based on these combined results, we propose that both composition and nutrient availability regulate DOM metabolism in Arctic aquatic ecosystems. Our empirical findings are incorporated into a mechanistic conceptual model highlighting two key enzymatic processes in the mineralization of riverine OM: (i) the role of phenol oxidase activity in reducing inhibitory phenolic compounds and (ii) the role of phosphatase in mobilizing organic P. Permafrost-derived DOM degradation was less constrained by this initial 'phenolic-OM' inhibition; thus, informing reports of high biological availability of ancient, permafrost-derived DOM with clear ramifications for its metabolism in fluvial networks and feedbacks to climate.

Optical properties and bioavailability of dissolved organic matter along a flow-path continuum from soil pore waters to the Kolyma River mainstem, East Siberia

“…Furthermore, selective processing and loss of permafrostderived DOM has been shown to occur via microbial metabolism throughout the Kolyma River basin, as waters move downstream through the fluvial network (Mann et al, 2014Spencer et al, 2015). Here, we complement these previous studies by providing extensive spatial characterization of DOM along a flow-path continuum from soil pore waters to the Kolyma River mainstem during midsummer (July) baseflow.…”

“…The higher overall amounts of bioavailable DOC we measured in soil pore waters may reflect a highly bioreactive permafrost or aged surface soil derived fraction of the bulk DOC pool (e.g., Vonk et al, 2013;Mann et al, 2014). Further downstream in larger tributary and Kolyma mainstem waters, it has been shown that lower total amounts of bioavailable DOC is supported almost entirely from predominantly modern radiocarbon aged surface soils and vegetation sources .…”

“…These assays relied upon 5-day biological oxygen demand (BOD) incubations, with methods similar to those in Mann et al (2014). Water samples were collected in triplicate glass 300 mL BOD bottles and filtered as DOC (above).…”

“…umn: (i) photochemical reactions, where DOM is degraded to CO 2 or to compounds bioavailable for bacterial uptake (Moran and Zepp, 1997;Laurion and Mladenov, 2013;Cory et al, 2014); (ii) flocculation of terrestrial DOM resulting in the settling of particulate organic matter (Wachenfeldt et al, 2009); (iii) loss via aggregation of DOM owing to changes in ionic strength when freshwater mixes with sea water (Sholkovitz, 1976); (iv) DOM sorption to particles and sedimentation (Chin et al, 1998); bacterial uptake and utilization of the bioavailable fraction (Bronk, 2002;Karl and Björkman, 2002;Mann et al, 2014;Spencer et al, 2015). Measurements of waters along a hydrologic flow path may provide unique insights into the characteristics of DOM as it is modified through these various processes along the soilstream-river continuum.…”

Bacterial production in subarctic peatland lakes enriched by thawing permafrost

“…4412 B. N. Deshpande et al: Bacterial production in thermokarst lakes 2009). The availability of organic substrates from these vast permafrost peatland environments to bacterial communities in aquatic ecosystems is likely to be influenced by a variety of factors, including the soil biogeochemical composition, particle and molecular size, and potentially other environmental factors, such as nutrient concentrations and temperature (Mann et al, 2014;Lapierre et al, 2013). Lakes in the boreal zone with flat catchments dominated by forest and peatland areas are strongly heterotrophic systems that have high rates of bacterial production (e.g., Kankaala et al, 2006), but less is known about the bacterial characteristics of peatland lakes further northwards, in permafrost regions.…”