Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Abstract

The long-term burial of organic carbon in sediments results in the net accumulation of oxygen in the atmosphere, thereby mediating the redox state of the Earth's biosphere and atmosphere. Sediment microbial activity plays a major role in determining whether particulate organic carbon is recycled or buried. A diverse consortium of microorganisms that hydrolyze, ferment, and terminally oxidize organic compounds mediates anaerobic organic matter mineralization in anoxic sediments. Variable temperature regulation of the sequential processes, leading from the breakdown of complex particulate organic carbon to the production and subsequent consumption of labile, low-molecular weight, dissolved intermediates, could play a key role in controlling rates of overall organic carbon mineralization. We examined sediment organic carbon cycling in a sediment slurry and in flow through bioreactor experiments. The data show a variable temperature response of the microbial functional groups mediating organic matter mineralization in anoxic marine sediments, resulting in the temperaturedriven decoupling of the production and consumption of organic intermediates. This temperature-driven decoupling leads to the accumulation of labile, low-molecular weight, dissolved organic carbon at low temperatures and low-molecular weight dissolved organic carbon limitation of terminal metabolism at higher temperatures.carbon cycle ͉ fermentation ͉ terminal metabolism ͉ sulfate reduction M icrobes performing the terminal mineralization of organic carbon to metabolic end products ( Fig. 1) are limited largely to labile, low-molecular weight (LMW), dissolved organic matter [LMW-dissolved organic carbon (DOC)] (molecular mass, Ͻ600 Da) that can be transported across cellular membranes (1). Particulate organic matter is initially broken down into high-molecular weight dissolved organic matter through extracellular enzymatic hydrolysis. High-molecular weight dissolved organic matter is further hydrolyzed and fermented to LMW-DOC, such as volatile fatty acids (VFAs) (2-4), that are available for terminal metabolism ( Fig. 1) (2,5,6). Despite the importance of hydrolysis͞fermentation in organic matter mineralization, relatively little is known about the environmental controls on this process.We examined the regulation of organic carbon mineralization in anoxic coastal marine sediments. A large fraction (55%) of global sediment organic matter oxidation occurs in coastal marine sediments, even though they account for only 7.5% of the total area of marine sediments (7,8). High metabolic rates in these sediments deplete oxygen within millimeters of the sediment-water interface, and the majority of organic matter mineralization proceeds via anaerobic pathways (9), mainly sulfate reduction (9-12). The organic carbon consumed by sulfatereducing bacteria is often VFAs, such as acetic acid (5, 6).Temperature and substrate availability influence the rates and seasonal patterns of microbial activity (13) and, hence, organic matter mineralization (14). For instance,...

Temperature induced decoupling of enzymatic hydrolysis and carbon remineralization in long-term incubations of Arctic and temperate sediments

“…The accumulation of DOC resistant to transformation or uptake is also in accordance with observations of DOC generated in short experiments conducted with coastal temperate sediments (Weston and Joye, 2005). In that study, passage of artificial anoxic porewater through bioreactors filled with temperate sediments collected at different seasons and incubated at the in situ temperatures of 12-29°C yielded an outflow of DOC from the bioreactors.…”

“…In Arctic sediments, substrate addition and/or homogenization also led to transient buildup of DOC constituents such as VFA (Brü chert and Arnosti, 2003;Arnosti et al, 2005), but within days to weeks, the accumulated DOC was consumed again. Short-term experiments with substrateamended coastal sediments also showed that production and consumption of DOC can become unbalanced over the temperature range typically experienced by temperate sediments (Weston and Joye, 2005).…”

“…In that study, passage of artificial anoxic porewater through bioreactors filled with temperate sediments collected at different seasons and incubated at the in situ temperatures of 12-29°C yielded an outflow of DOC from the bioreactors. Less than half of the DOC generated within the bioreactors was remineralized by sulfate reducers, leading Weston and Joye (2005) to conclude that the DOC was refractory, on the 10-day timescale of the experiment. Although the bioreactor experiments could not be used to distinguish between hydrolytic and fermentative steps, the data from our temperate and Arctic sediments suggest that the 'sticking point' might be found within the fermentative community.…”

The Correlations Between Mercury Speciation and Dissolved Organic Matter in the Sediment of the Red Sea

“…Values of CarbonNitrogen atomic ratio (C/N) suggests an organic matter input derived from vascular plants (Meyers, 1994), characterized by limiting nitrate concentration (Mari et al, 2001). The mean value of our study (C/N = 1.41 ± 0.34) is lower the Redfield ratio (C/N = 5.7; Gordon and Goni, 2004;Weston and Joye, 2005). The TN of the sediments avoids being remineralized into the water column by adsorption to the mineral clay surface, hence recording smaller C/N ratios (Stevenson and Cheng, 1972;Suthhof et al, 2000) that are explained by selective degradation of the organic compounds and by immobilization of N by microorganisms during early diagenesis (Meyers, 1994).…”

Summary of carbon, nitrogen, and iron leaching characteristics and fluorescence properties of materials considered for subseafloor observatory assembly

“…At the end of all incubations, sample fluid was frozen until subsequent dissolved organic carbon (DOC) and total dissolved nitrogen (TDN) analysis. DOC and TDN concentrations were measured in the Joye Geochemistry Analytical Laboratory at the University of Georgia (USA) according to published protocols (Weston and Joye, 2005). Briefly, 10 mL of fluid from the leaching experiments was transferred into acid-washed, combusted autosampler vials.…”