Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments
Humic substances are redox-active organic molecules, which play pivotal roles in several biogeochemical cycles due to their electron-transferring capacity involving multiple abiotic and microbial transformations. Based on the redox properties of humic substances, and the metabolic capabilities of mi...
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doaj-d2c549a9c95f46a0aae416957cd3f0032020-11-25T03:08:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-04-011110.3389/fmicb.2020.00587510582Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland SedimentsEdgardo I. Valenzuela0Claudia Padilla-Loma1Nicolás Gómez-Hernández2Nguyen E. López-Lozano3Sergio Casas-Flores4Francisco J. Cervantes5División de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, San Luis Potosí, MexicoDivisión de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, San Luis Potosí, MexicoDivisión de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, San Luis Potosí, MexicoDivisión de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, San Luis Potosí, MexicoDivisión de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, San Luis Potosí, MexicoLaboratory for Research on Advanced Processes for Water Treatment, Engineering Institute, Campus Juriquilla, Universidad Nacional Autónoma de México, Querétaro, MexicoHumic substances are redox-active organic molecules, which play pivotal roles in several biogeochemical cycles due to their electron-transferring capacity involving multiple abiotic and microbial transformations. Based on the redox properties of humic substances, and the metabolic capabilities of microorganisms to reduce and oxidize them, we hypothesized that they could mediate the anaerobic oxidation of methane (AOM) coupled to the reduction of nitrous oxide (N2O) in wetland sediments. This study provides several lines of evidence indicating the coupling between AOM and the reduction of N2O through an extracellular electron transfer mechanism mediated by the redox active functional groups in humic substances (e.g., quinones). We found that the microbiota of a sediment collected from the Sisal wetland (Yucatán Peninsula, southeastern Mexico) was able to reduce N2O (4.6 ± 0.5 μmol N2O g sed.–1 day–1) when reduced humic substances were provided as electron donor in a close stoichiometric relationship. Furthermore, a microbial enrichment derived from the wetland sediment achieved simultaneous 13CH4 oxidation (1.3 ± 0.1 μmol 13CO2 g sed.–1 day–1) and N2O reduction (25.2 ± 0.5 μmol N2O g sed.–1 day–1), which was significantly dependent on the presence of humic substances as an extracellular electron shuttle. Taxonomic characterization based on 16S rRNA gene sequencing revealed Acinetobacter (a ɣ-proteobacterium), the Rice Cluster I from the Methanocellaceae and an uncultured archaeon from the Methanomicrobiaceae family as the microbes potentially involved in AOM linked to N2O reduction mediated by humic substances. The findings reported here suggest that humic substances might play an important role to prevent the emission of greenhouse gases (CH4 and N2O) from wetland sediments. Further efforts to evaluate the feasibility of this novel mechanism under the natural conditions prevailing in ecosystems must be considered in future studies.https://www.frontiersin.org/article/10.3389/fmicb.2020.00587/fullgreenhouse gasesanaerobic methanotrophywetlandsnitrous oxideextracellular electron transfernatural organic matter |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Edgardo I. Valenzuela Claudia Padilla-Loma Nicolás Gómez-Hernández Nguyen E. López-Lozano Sergio Casas-Flores Francisco J. Cervantes |
spellingShingle |
Edgardo I. Valenzuela Claudia Padilla-Loma Nicolás Gómez-Hernández Nguyen E. López-Lozano Sergio Casas-Flores Francisco J. Cervantes Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments Frontiers in Microbiology greenhouse gases anaerobic methanotrophy wetlands nitrous oxide extracellular electron transfer natural organic matter |
author_facet |
Edgardo I. Valenzuela Claudia Padilla-Loma Nicolás Gómez-Hernández Nguyen E. López-Lozano Sergio Casas-Flores Francisco J. Cervantes |
author_sort |
Edgardo I. Valenzuela |
title |
Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments |
title_short |
Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments |
title_full |
Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments |
title_fullStr |
Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments |
title_full_unstemmed |
Humic Substances Mediate Anaerobic Methane Oxidation Linked to Nitrous Oxide Reduction in Wetland Sediments |
title_sort |
humic substances mediate anaerobic methane oxidation linked to nitrous oxide reduction in wetland sediments |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2020-04-01 |
description |
Humic substances are redox-active organic molecules, which play pivotal roles in several biogeochemical cycles due to their electron-transferring capacity involving multiple abiotic and microbial transformations. Based on the redox properties of humic substances, and the metabolic capabilities of microorganisms to reduce and oxidize them, we hypothesized that they could mediate the anaerobic oxidation of methane (AOM) coupled to the reduction of nitrous oxide (N2O) in wetland sediments. This study provides several lines of evidence indicating the coupling between AOM and the reduction of N2O through an extracellular electron transfer mechanism mediated by the redox active functional groups in humic substances (e.g., quinones). We found that the microbiota of a sediment collected from the Sisal wetland (Yucatán Peninsula, southeastern Mexico) was able to reduce N2O (4.6 ± 0.5 μmol N2O g sed.–1 day–1) when reduced humic substances were provided as electron donor in a close stoichiometric relationship. Furthermore, a microbial enrichment derived from the wetland sediment achieved simultaneous 13CH4 oxidation (1.3 ± 0.1 μmol 13CO2 g sed.–1 day–1) and N2O reduction (25.2 ± 0.5 μmol N2O g sed.–1 day–1), which was significantly dependent on the presence of humic substances as an extracellular electron shuttle. Taxonomic characterization based on 16S rRNA gene sequencing revealed Acinetobacter (a ɣ-proteobacterium), the Rice Cluster I from the Methanocellaceae and an uncultured archaeon from the Methanomicrobiaceae family as the microbes potentially involved in AOM linked to N2O reduction mediated by humic substances. The findings reported here suggest that humic substances might play an important role to prevent the emission of greenhouse gases (CH4 and N2O) from wetland sediments. Further efforts to evaluate the feasibility of this novel mechanism under the natural conditions prevailing in ecosystems must be considered in future studies. |
topic |
greenhouse gases anaerobic methanotrophy wetlands nitrous oxide extracellular electron transfer natural organic matter |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.00587/full |
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