Humic substances as fully regenerable electron acceptors in recurrently anoxic environments

Klüpfel, Laura; Piepenbrock, Annette; Kappler, Andreas; Sander, Michael

doi:10.1038/ngeo2084

Cited by 468 publications

(344 citation statements)

References 27 publications

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“…The potential role of HS is further emphasized, because their electron-accepting capacity is fully recycled in recurrently anoxic environments. Thus, the suppression of methanogenesis by HS may be much greater than previously considered (it had been estimated to be on the order of 190,000 mol CH 4 · km Ϫ2 · year Ϫ1 [43]). …”

Section: Discussionmentioning

confidence: 92%

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Valenzuela

Prieto-Davó

López-Lozano

et al. 2017

Appl Environ Microbiol

132

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Wetlands constitute the main natural source of methane on Earth due to their high content of natural organic matter (NOM), but key drivers, such as electron acceptors, supporting methanotrophic activities in these habitats are poorly understood. We performed anoxic incubations using freshly collected sediment, along with water samples harvested from a tropical wetland, amended with 13 C-methane (0.67 atm) to test the capacity of its microbial community to perform anaerobic oxidation of methane (AOM) linked to the reduction of the humic fraction of its NOM. Collected evidence demonstrates that electron-accepting functional groups (e.g., quinones) present in NOM fueled AOM by serving as a terminal electron acceptor. Indeed, while sulfate reduction was the predominant process, accounting for up to 42.5% of the AOM activities, the microbial reduction of NOM concomitantly occurred. Furthermore, enrichment of wetland sediment with external NOM provided a complementary electron-accepting capacity, of which reduction accounted for ϳ100 nmol 13 CH 4 oxidized · cm Ϫ3 · day Ϫ1 . Spectroscopic evidence showed that quinone moieties were heterogeneously distributed in the wetland sediment, and their reduction occurred during the course of AOM. Moreover, an enrichment derived from wetland sediments performing AOM linked to NOM reduction stoichiometrically oxidized methane coupled to the reduction of the humic analogue anthraquinone-2,6-disulfonate. Microbial populations potentially involved in AOM coupled to microbial reduction of NOM were dominated by divergent biota from putative AOMassociated archaea. We estimate that this microbial process potentially contributes to the suppression of up to 114 teragrams (Tg) of CH 4 · year Ϫ1 in coastal wetlands and more than 1,300 Tg · year Ϫ1 , considering the global wetland area. IMPORTANCEThe identification of key processes governing methane emissions from natural systems is of major importance considering the global warming effects triggered by this greenhouse gas. Anaerobic oxidation of methane (AOM) coupled to the microbial reduction of distinct electron acceptors plays a pivotal role in mitigating methane emissions from ecosystems. Given their high organic content, wetlands constitute the largest natural source of atmospheric methane. Nevertheless, processes controlling methane emissions in these environments are poorly understood. Here, we provide tracer analysis with 13 CH 4 and spectroscopic evidence revealing that AOM linked to the microbial reduction of redox functional groups in natural organic matter (NOM) prevails in a tropical wetland. We suggest that microbial reduction of NOM may largely contribute to the suppression of methane emissions from

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Section: Discussionmentioning

confidence: 92%

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Valenzuela

Prieto-Davó

López-Lozano

et al. 2017

Appl Environ Microbiol

132

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“…The EA-induced decrease in CH 4 production was much more likely due to outcompetition of the methanogens for methanogenic substrates by anaerobically respiring bacteria (Klüpfel et al 2014 production could also be due to anaerobic respiration coupled with EAs with a lower reduction potential. The negligible effect of NO 3 -and SO 4 2-on the potential net CH 4 production in the two deepest layers (P 90-130 and P 390-410 ) of the profundal zone (Table 2) is probably due to the relatively low number of competing anaerobically respiring bacteria.…”

Section: Production Of Ch 4 and Ticmentioning

confidence: 99%

“…EAs can directly inhibit methanogenesis (Klüber and Conrad 1998) or decrease/suppress it by diverting the flow of electrons (from H 2 , volatile fatty acids, alcohols) generated by fermentative bacteria from methanogenic to other anaerobic respiration pathways (Klüpfel et al 2014). EAs can also increase CH 4 consumption via CH 4 oxidation (á Norði and Thamdrup 2014).…”

Section: Introductionmentioning

confidence: 99%

Effects of alternative electron acceptors on the activity and community structure of methane-producing and consuming microbes in the sediments of two shallow boreal lakes

Rissanen

Karvinen

Nykänen

et al. 2017

FEMS Microbiology Ecology

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“…Due to thermodynamic controls, CH 4 production is only competitive upon depletion of alternative, energetically more favorable electron acceptors for anaerobic respiration, such as nitrate, iron, sulfate, or oxidized humics (Blodau, 2002;Klüpfel et al, 2014). CH 4 is predominantly produced via two pathways: hydrogenotrophic and acetoclastic methanogenesis.…”

Section: Introductionmentioning

confidence: 99%

Differential response of carbon cycling to long-term nutrient input and altered hydrological conditions in a continental Canadian peatland

et al. 2018

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Abstract. Peatlands play an important role in global carbon cycling, but their responses to long-term anthropogenically changed hydrologic conditions and nutrient infiltration are not well known. While experimental manipulation studies, e.g., fertilization or water table manipulations, exist on the plot scale, only few studies have addressed such factors under in situ conditions. Therefore, an ecological gradient from the center to the periphery of a continental Canadian peatland bordering a eutrophic water reservoir, as reflected by increasing nutrient input, enhanced water level fluctuations, and increasing coverage of vascular plants, was used for a case study of carbon cycling along a sequence of four differently altered sites. We monitored carbon dioxide (CO 2 ) and methane (CH 4 ) surface fluxes and dissolved inorganic carbon (DIC) and CH 4 concentrations in peat profiles from April 2014 through September 2015. Moreover, we studied bulk peat and pore-water quality and we applied δ 13 C-CH 4 and δ 13 C-CO 2 stable isotope abundance analyses to examine dominant CH 4 production and emission pathways during the growing season of 2015. We observed differential responses of carbon cycling at the four sites, presumably driven by abundances of plant functional types and vicinity to the reservoir. A shrub-dominated site in close vicinity to the reservoir was a comparably weak sink for CO 2 (in 1.5 years: −1093 ± 794, in 1 year: +135 ± 281 g CO 2 m −2 ; a net release) as compared to two graminoid-moss-dominated sites and a moss-dominated site (in 1.5 years: −1552 to −2260 g CO 2 m −2 , in 1 year: −896 to −1282 g CO 2 m −2 ). Also, the shrub-dominated site featured notably low DIC pore-water concentrations and comparably 13 C-enriched CH 4 (δ 13 C-CH 4 : −57.81 ± 7.03 ‰) and depleted CO 2 (δ 13 C-CO 2 : −15.85 ± 3.61 ‰) in a more decomposed peat, suggesting a higher share of CH 4 oxidation and differences in predominant methanogenic pathways. In comparison to all other sites, the graminoid-mossdominated site in closer vicinity to the reservoir featured a ∼ 30 % higher CH 4 emission (in 1.5 years: +61.4 ± 32, in 1 year: +39.86 ± 16.81 g CH 4 m −2 ). Low δ 13 C-CH 4 signatures (−62.30 ± 5.54 ‰) indicated only low mitigation of CH 4 emissions by methanotrophic activity here. Pathways of methanogenesis and methanotrophy appeared to be related to the vicinity to the water reservoir: the importance of acetoclastic CH 4 production apparently increased toward the reservoir, whereas the importance of CH 4 oxidation increased toward the peatland center. Plant-mediated transport was the prevailing CH 4 emission pathway at all sites even where graminoids were rare. Our study thus illustrates accelerated carbon cycling in a strongly altered peatland with consequences for CO 2 and CH 4 budgets. However, our results suggest that long-term excess nutrient input does not necessarily lead to a loss of the peatland carbon sink function.

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Humic substances as fully regenerable electron acceptors in recurrently anoxic environments

Cited by 468 publications

References 27 publications

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Effects of alternative electron acceptors on the activity and community structure of methane-producing and consuming microbes in the sediments of two shallow boreal lakes

Differential response of carbon cycling to long-term nutrient input and altered hydrological conditions in a continental Canadian peatland

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