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Title: Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands

Abstract

Inland waters are increasingly recognized as critical sites of methane emissions to the atmosphere, but the biogeochemical reactions driving such fluxes are less well understood. The Prairie Pothole Region (PPR) of North America is one of the largest wetland complexes in the world, containing millions of small, shallow wetlands. The sediment pore waters of PPR wetlands contain some of the highest concentrations of dissolved organic carbon (DOC) and sulfur species ever recorded in terrestrial aquatic environments. Using a suite of geochemical and microbiological analyses we measured the impact of sedimentary carbon and sulfur transformations in these wetlands on methane fluxes to the atmosphere. This research represents the first study of coupled geochemistry and microbiology within the PPR, and demonstrates how the conversion of abundant labile DOC pools into methane results in some of the highest fluxes of this greenhouse gas to the atmosphere ever reported. Abundant DOC and sulfate additionally supported some of the highest sulfate reduction rates ever measured in terrestrial aquatic environments, which we infer to account for a large fraction of carbon mineralization in this system. Methane accumulations in zones of active sulfate reduction may be due to either the transport of free methane gas from deepermore » locations, or the co-occurrence of methanogenesis and sulfate reduction. If both respiratory processes are concurrent, any competitive inhibition of methanogenesis by sulfate-reducing bacteria may be lessened by the presence of large labile DOC pools that yield non-competitive substrates such as methanol. Our results reveal some of the underlying mechanisms that make PPR wetlands biogeochemical hotspots, which ultimately leads to their critical, but poorly recognized role in regional greenhouse gas emissions.« less

Authors:
 [1];  [2];  [3];  [4];  [2];  [3];  [3];  [5];  [5];  [3];  [1];  [5]; ORCiD logo [6]
  1. Microbiology Department, The Ohio State University, Columbus OH 43210 USA
  2. Environmental Molecular Sciences Laboratory, Richland WA 99350 USA
  3. United States Geological Survey - Northern Prairie Wildlife Research Center, Jamestown ND 58401 USA
  4. United States Geological Survey, Crustal Geophysics and Geochemistry Science Center, Building 20, Denver Federal Center Denver CO 80225 USA
  5. School of Earth Sciences, The Ohio State University, Columbus OH 43210 USA
  6. Microbiology Department, The Ohio State University, Columbus OH 43210 USA; School of Earth Sciences, The Ohio State University, Columbus OH 43210 USA
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406680
Report Number(s):
PNNL-SA-120033
Journal ID: ISSN 1354-1013; 48837; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Global Change Biology; Journal Volume: 23; Journal Issue: 8
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Dalcin Martins, Paula, Hoyt, David W., Bansal, Sheel, Mills, Christopher T., Tfaily, Malak, Tangen, Brian A., Finocchiaro, Raymond G., Johnston, Michael D., McAdams, Brandon C., Solensky, Matthew J., Smith, Garrett J., Chin, Yu-Ping, and Wilkins, Michael J. Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands. United States: N. p., 2017. Web. doi:10.1111/gcb.13633.
Dalcin Martins, Paula, Hoyt, David W., Bansal, Sheel, Mills, Christopher T., Tfaily, Malak, Tangen, Brian A., Finocchiaro, Raymond G., Johnston, Michael D., McAdams, Brandon C., Solensky, Matthew J., Smith, Garrett J., Chin, Yu-Ping, & Wilkins, Michael J. Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands. United States. doi:10.1111/gcb.13633.
Dalcin Martins, Paula, Hoyt, David W., Bansal, Sheel, Mills, Christopher T., Tfaily, Malak, Tangen, Brian A., Finocchiaro, Raymond G., Johnston, Michael D., McAdams, Brandon C., Solensky, Matthew J., Smith, Garrett J., Chin, Yu-Ping, and Wilkins, Michael J. Thu . "Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands". United States. doi:10.1111/gcb.13633.
@article{osti_1406680,
title = {Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in Prairie Pothole Wetlands},
author = {Dalcin Martins, Paula and Hoyt, David W. and Bansal, Sheel and Mills, Christopher T. and Tfaily, Malak and Tangen, Brian A. and Finocchiaro, Raymond G. and Johnston, Michael D. and McAdams, Brandon C. and Solensky, Matthew J. and Smith, Garrett J. and Chin, Yu-Ping and Wilkins, Michael J.},
abstractNote = {Inland waters are increasingly recognized as critical sites of methane emissions to the atmosphere, but the biogeochemical reactions driving such fluxes are less well understood. The Prairie Pothole Region (PPR) of North America is one of the largest wetland complexes in the world, containing millions of small, shallow wetlands. The sediment pore waters of PPR wetlands contain some of the highest concentrations of dissolved organic carbon (DOC) and sulfur species ever recorded in terrestrial aquatic environments. Using a suite of geochemical and microbiological analyses we measured the impact of sedimentary carbon and sulfur transformations in these wetlands on methane fluxes to the atmosphere. This research represents the first study of coupled geochemistry and microbiology within the PPR, and demonstrates how the conversion of abundant labile DOC pools into methane results in some of the highest fluxes of this greenhouse gas to the atmosphere ever reported. Abundant DOC and sulfate additionally supported some of the highest sulfate reduction rates ever measured in terrestrial aquatic environments, which we infer to account for a large fraction of carbon mineralization in this system. Methane accumulations in zones of active sulfate reduction may be due to either the transport of free methane gas from deeper locations, or the co-occurrence of methanogenesis and sulfate reduction. If both respiratory processes are concurrent, any competitive inhibition of methanogenesis by sulfate-reducing bacteria may be lessened by the presence of large labile DOC pools that yield non-competitive substrates such as methanol. Our results reveal some of the underlying mechanisms that make PPR wetlands biogeochemical hotspots, which ultimately leads to their critical, but poorly recognized role in regional greenhouse gas emissions.},
doi = {10.1111/gcb.13633},
journal = {Global Change Biology},
number = 8,
volume = 23,
place = {United States},
year = {Thu Feb 23 00:00:00 EST 2017},
month = {Thu Feb 23 00:00:00 EST 2017}
}
  • The activity of and potential substrates for methane-producing bacteria and sulfate-reducing bacteria were examined in marsh, estuary, and beach intertidal sediments. Slow rates of methane production were detected in all sediments, although rates of sulfate reduction were 100- to 1,000-fold higher. After sulfate was depleted in sediments, the rates of methane production sharply increased. The addition of methylamine stimulated methanogenesis in the presence of sulfate, and (/sup 14/C)methylamine was rapidly converted to /sup 14/CH/sub 4/ and /sup 14/CO/sub 2/ in freshly collected marsh sediment. Acetate, hydrogen, or methionine additions did not stimulate methanogenesis. (methyl-/sup 14/C)methionine and (2-/sup 14/C)acetate were convertedmore » to /sup 14/CO/sub 2/ and not to /sup 14/CH/sub 4/ in fresh sediment. No reduction of /sup 14/CO/sub 2/ to /sup 14/CH/sub 4/ occurred in fresh sediment. Molybdate, an inhibitor of sulfate reduction, inhibited (2-/sup 14/C)acetate metabolism by 98.5%. Fluoracetate, an inhibitor of acetate metabolism, inhibited sulfate reduction by 61%. These results suggest that acetate is a major electron donor for sulfate reduction in marine sediments. In the presence of high concentrations of sulfate, methane may be derived from novel substrates such as methylamine.« less
  • Rates of methane production (both acetate fermentation and CO{sub 2} reduction) and sulfate reduction were directly measured as a function of depth in the sediments of Lake Washington. Although methanogenesis was the primary mode of anaerobic respiration (63%), the major zone of methane production existed only below the sulfate reduction zone (16 cm). Acetate fermentation accounted for 61 to 85% of the total methane production, which is consistent with other low sulfate environments. The observed spatial separation of methane production and sulfate reduction, which has been reported for marine sediments, is attributed to competition between the methane-producing and sulfate-reducing bacteriamore » for acetate and hydrogen. This hypothesis is supported by the strong correlation between the measured distributions of acetate and hydrogen and the rates of methane produced from these two precursors in Lake Washington sediments. Acetate concentrations increased rapidly (from 10-16 {mu}M to 30-40 {mu}M) once the sulfate concentration decreased below 30 {mu}M and methane production via acetate fermentation began. A similar trend was observed for hydrogen concentrations, which increased from 7 to 22 nM up to 40 to 55 nM, at the onset of methanogenesis from CO{sub 2} and H{sub 2} (sulfate concentrations of 35-40 {mu}M). These results show, for the first time in a freshwater lake, the separation of methane production and sulfate reduction and the corresponding changes in acetate and hydrogen concentrations.« less
  • Cited by 2
  • Cited by 1
  • Surface sediments (0-10 cm) collected in 1980 and 1981 from 13 wetland areas in Iowa, Montana, Nebraska, North Dakota, and South Dakota were analyzed for total concentrations of arsenic, cadmium, lead, mercury, and selenium. Sediments from pothole-type wetlands had significantly higher concentrations of arsenic, cadmium, lead, and selenium than those from riverine wetlands. Mean (and range) of dry weight concentrations (mg/kg) for pothole and riverine locations, respectively, were arsenic, 4.4 (1.4-9.3) and 2.4 (0.7-6.1); cadmium 0.52 (0.17-0.87) and 0.26 (0.01-0.55); lead, 13 (7.4-22) and 6.6 (1.1-14); selenium, 0.89 (0.13-2.1) and 0.52(0.03-0.51). Mercury concentrations in sediment did not differ significantly betweenmore » pothole and riverine type wetlands (mean, 0.03, range 0.01-0.08). A comparison of the concentrations of elements found in this study with values reported in the literature indicated that, with the possible exception of location, levels were within normal or background ranges. 31 references, 1 figure, 3 tables.« less