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 ∼100 nmol ¹³ CH ₄ oxidized · cm ⁻³ · day ⁻¹ . 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 AOM-associated archaea. We estimate that this microbial process potentially contributes to the suppression of up to 114 teragrams (Tg) of CH ₄ · year ⁻¹ in coastal wetlands and more than 1,300 Tg · year ⁻¹ , considering the global wetland area. IMPORTANCE The 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 tropical wetlands. This is a novel avenue within the carbon cycle in which slowly decaying NOM (e.g., humic fraction) in organotrophic environments fuels AOM by serving as a terminal electron acceptor.

The OMEGA/Mars Express hyperspectral imager identified gypsum at several sites on Mars in 2005. These minerals constitute a direct record of past aqueous activity and are important with regard to the search of extraterrestrial life. Gale Crater was chosen as Mars Science Laboratory Curiosity's landing site because it is rich in gypsum, as are some desert soils of the Cuatro Ciénegas Basin (CCB) (Chihuahuan Desert, Mexico). The gypsum of the CCB, which is overlain by minimal carbonate deposits, was the product of magmatic activity that occurred under the Tethys Sea. To examine this Mars analogue, we retrieved gypsum-rich soil samples from two contrasting sites with different humidity in the CCB. To characterize the site, we obtained nutrient data and analyzed the genes related to the N cycle (nifH, nirS, and nirK) and the bacterial community composition by using 16S rRNA clone libraries. As expected, the soil content for almost all measured forms of carbon, nitrogen, and phosphorus were higher at the more humid site than at the drier site. What was unexpected is the presence of a rich and divergent community at both sites, with higher taxonomic diversity at the humid site and almost no taxonomic overlap. Our results suggest that the gypsum-rich soils of the CCB host a unique microbial ecosystem that includes novel microbial assemblies.

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.

Due to the environmental conditions presented in arid zones, it is expected to have a high influence of deterministic processes over the community assemblages. Symbiotic interactions with microorganisms could increase colonization and survival of plants in difficult conditions, independent of the plants physiological and morphological characteristics. In this context, the microbial communities associated to plants that inhabit these types of areas can be a good model to understand the community assembly processes. We investigated the influence of stochastic and deterministic processes in the assemblage of rhizosphere microbial communities of Agave lechuguilla and bulk soil on the Cuatro Cienegas Basin, a site known for its oligotrophic conditions. We hypothesize that rhizospheric microbial communities of A. lechuguilla differ from those of bulk soil as they differ in physicochemical properties of soil and biotic interactions, including not only the plant, but also their microbial co-occurrence networks, it is expected that microbial species usually critical for plant growth and health are more common in the rhizosphere, whereas in the bulk soil microbial species related to the resistance to abiotic stress are more abundant. In order to confirm this hypothesis, 16S rRNA gene was sequenced by Illumina from rhizospheric and bulk soil samples in two seasons, also the physicochemical properties of the soil were determined. Our results showed differences in bacterial diversity, community composition, potential functions, and interaction networks between the rhizosphere samples and the ones from bulk soil. Although community structure arises from a complex interplay between deterministic and stochastic forces, our results suggest that A. lechuguilla recruits specific rhizospheric microbes with functional traits that benefits the plant through growth promotion and nutrition. This selection follows principally a deterministic process that shapes the rhizospheric microbial communities, directed by the plant modifications around the roots but also subjected to the influence of other environmental variables, such as seasonality and soil properties. Interestingly, keystone taxa in the interactions networks, not necessarily belong to the most abundant taxonomic groups, but they have an important role by their functional traits and keeping the connections on the community network.