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Article Is Available Online Standing That Under the Correct Conditions, Microbes Can Pro- At Biogeosciences, 15, 1733–1747, 2018 https://doi.org/10.5194/bg-15-1733-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 4.0 License. Molecular characterization of organic matter mobilized from Bangladeshi aquifer sediment: tracking carbon compositional change during microbial utilization Lara E. Pracht1, Malak M. Tfaily2, Robert J. Ardissono1, and Rebecca B. Neumann1 1Department of Civil and Environmental Engineering, University of Washington, Seattle, 98195, USA 2Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, 99354, USA Correspondence: Rebecca B. Neumann ([email protected]) Received: 29 June 2017 – Discussion started: 11 July 2017 Revised: 1 March 2018 – Accepted: 2 March 2018 – Published: 26 March 2018 Abstract. Bioavailable organic carbon in aquifer recharge In anaerobic environments, energy yields from redox reac- waters and sediments can fuel microbial reactions with im- tions are small and the amount of energy required to re- plications for groundwater quality. A previous incubation move electrons from highly reduced carbon substrates during experiment showed that sedimentary organic carbon (SOC) oxidation decreases the thermodynamic favorability of de- mobilized off sandy sediment collected from an arsenic- grading compounds with a low NOSC. While all compound contaminated and methanogenic aquifer in Bangladesh was types were eventually degraded during incubation, NOSC bioavailable; it was transformed into methane. We used and compound size controlled the rates of carbon transforma- high-resolution mass spectrometry to molecularly character- tion. Large, more thermodynamically favorable compounds ize this mobilized SOC, reference its composition against (e.g., aromatics with a high NOSC) were targeted first, while dissolved organic carbon (DOC) in surface recharge water, small, less thermodynamically favorable compounds (e.g., track compositional changes during incubation, and advance alkanes and olefinics with a low NOSC) were used last. understanding of microbial processing of organic carbon These results indicate that in anaerobic conditions, microbial in anaerobic environments. Organic carbon mobilized off communities are capable of degrading and mineralizing all aquifer sediment was more diverse, proportionately larger, forms of organic matter, converting larger energy-rich com- more aromatic, and more oxidized than DOC in surface pounds into smaller energy-poor compounds. However, in an recharge. Mobilized SOC was predominately composed of open system, where fresh carbon is continually supplied, the terrestrially derived organic matter and had characteristics slower degradation rate of reduced carbon compounds would signifying that it evaded microbial processing within the enable this portion of the organic carbon pool to build up, ex- aquifer. Approximately 50 % of identified compounds in mo- plaining the apparent persistence of compounds with a low bilized SOC and in DOC from surface recharge water con- NOSC in anaerobic environments. tained sulfur. During incubation, after mobilized SOC was converted into methane, new organosulfur compounds with high S-to-C ratios and a high nominal oxidation state of car- 1 Introduction bon (NOSC) were detected. We reason that these detected compounds formed abiotically following microbial reduction Organic carbon can impact groundwater quality both posi- of sulfate to sulfide, which could have occurred during incu- tively and negatively by fueling microbial reactions that re- bation but was not directly measured or that they were mi- move and contribute dissolved contaminants to groundwater crobially synthesized. Most notably, microbes transformed (e.g., natural attenuation of nitrate, mobilization of geogenic all carbon types during incubation, including those currently arsenic, methane production). The organic carbon fueling considered thermodynamically unviable for microbes to de- these microbial reactions can come from the near-surface en- grade in anaerobic conditions (i.e., those with a low NOSC). vironment, transported into the aquifer with recharging water Published by Copernicus Publications on behalf of the European Geosciences Union. 1734 L. E. Pracht et al.: Molecular characterization of organic matter mobilized from Bangladeshi aquifer sediment (LeBlanc, 1984; Mailloux et al., 2013; Neumann et al., 2010) Postma, 1994; Postma et al., 2012). With contemporary un- or can reside in the aquifer sediment, co-deposited when the derstanding of the factors that control carbon bioavailability, aquifer formed (Korom, 1992; Parkin and Simpkins, 1995; this diminishment in reactivity can be attributed to the devel- Postma et al., 2007). Ultimately, the extent to which these opment of constraints limiting microbial processing of sedi- sources of organic carbon can fuel subsurface reactions de- mentary organic carbon rather than to a complete absence of pends on their availability to the resident microbial commu- SOC. Results from an incubation experiment conducted with nity. sediments collected from a methanogenic, alluvial aquifer in Historically, it was thought that molecular structure dic- Munshiganj, Bangladesh, align with such an interpretation tated carbon bioavailability (Lehmann and Kleber, 2015; (Neumann et al., 2014). Sampling and homogenization of Lutzow et al., 2006; Schmidt et al., 2011). Simple monomers the aquifer sediments mobilized 0.33 ± 0.06 mg C of organic were considered bioavailable, while more complex com- carbon per gram of sediment or 8.8 ± 0.7 % of total SOC pounds, particularly those with aromatic rings, were con- (Sect. S1 in the Supplement). During incubation, the mobi- sidered molecularly recalcitrant. However, it is now under- lized SOC was rapidly converted into methane by the native stood that given the correct conditions, microbes can process microbial community (Neumann et al., 2014). The experi- all carbon types, continually transforming large, energy-rich ment demonstrated that the ∼ 5000 year old, sandy aquifer organic compounds into smaller, energy-poor organic com- sediments contain a notable amount of organic carbon that, if pounds (Lehmann and Kleber, 2015). In fact, compounds mobilized within the aquifer, could fuel microbial reactions. previously considered recalcitrant often have rapid turnover In the Neumann et al. (2014) incubation experiment, SOC rates (Amelung et al., 2008). was mobilized during sampling and/or homogenization of The current view is that accessibility and microbial ecol- the aquifer sediment. While this type of physical disturbance ogy control carbon bioavailability (Lehmann and Kleber, to the aquifer matrix could not occur in situ (i.e., within the 2015; Schmidt et al., 2011). Physical protection mechanisms, aquifer), it is plausible that more realistic aquifer perturba- such as organic carbon sorption to mineral surfaces and en- tions, such as geochemical changes brought about by large- capsulation into hydrophobic biopolymers or regions, can scale groundwater pumping, could mobilize SOC in situ. For limit microbial access to carbon (Baldock and Skjemstad, example, mineral-associated organic carbon can become mo- 2000; Petridis et al., 2014), and energetic constraints, nutri- bilized into groundwater if solution pH increases (Gu et al., ent limitations, and metabolic capacities of microbial com- 1994; Jardine et al., 1989; Kaiser and Zech, 1999), if concen- munities can affect the ability of microbes to process dif- trations of ions that compete with organic carbon for sorption ferent chemical forms of organic carbon (Fontaine et al., sites increase (Jardine et al., 1989; Kaiser and Zech, 1999), or 2007; LaRowe and Van Cappellen, 2011; Trulleyova and Ru- if an influx of dissolved organic carbon fuels microbial reac- lik, 2004). Recent work has demonstrated that in anaerobic tions that target the mineral phase (e.g., reductive dissolution settings, the nominal oxidation state of carbon (NOSC) in- of iron oxide minerals) (Eusterhues et al., 2003; Fontaine et fluences bioavailability. In a sulfate-reducing aquifer, com- al., 2007; Mikutta et al., 2006). pounds with a high NOSC were missing, while those with a At two different sites in Asia, there is published evi- low NOSC persisted (Boye et al., 2017). This outcome re- dence that large-scale groundwater pumping has facilitated flects the fact that organic carbon oxidation (i.e., removing the mobilization of sedimentary organic carbon. At the site electrons from carbon) requires energy (LaRowe and Van in Bangladesh where materials for the Neumann et al. (2014) Cappellen, 2011), which must be offset by energy released incubation were collected, dry-season groundwater irriga- from the reduction half-reaction. The amount of energy re- tion has pulled surface recharge water down to a 30 m depth quired to fully oxidize a carbon compound increases with the where irrigation wells are screened (Harvey et al., 2006). number of electrons. Thus, in anaerobic conditions, where Field measurements showed that dissolved organic carbon the amount of energy released from reduction half-reactions (DOC) concentrations in groundwater remained constant is lower than that in oxic conditions, it is, paradoxically, more down to this depth but that DOC age increased (Harvey et thermodynamically favorable to oxidize compounds with a al., 2002). This situation is only possible if SOC was re- high NOSC than compounds with a low NOSC (Keiluweit leased along the groundwater flow path as younger DOC et al., 2016). It
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