Response of a methane-driven interaction network to stressor intensification

Ho, Adrian; Mendes, Lucas William; Lee, Hyo‐Jung; Kaupper, Thomas; Mo, Yongliang; Bodelier, Paul L. E.; Jia, Zhongjun; Horn, Marcus A.

doi:10.1093/femsec/fiaa180

Cited by 21 publications

(33 citation statements)

References 80 publications

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“…Similarly, aerobic methanotrophs may also rely on Sphagnum for molecular oxygen, enabling their proliferation in anoxic niches in peatland ecosystems (Raghoebarsing et al, 2005;Ho and Bodelier, 2015); or independently relying on incomplete denitrification (van Grinsven et al, 2020). The interaction of aerobic methanotrophs with their biotic environment, appears to be relevant in modulating community functioning, and may help confer resilience during disturbances prompting the use of alternative strategies and the formation of synergistic/antagonistic interactions (Ho et al, 2014(Ho et al, , 2016(Ho et al, , 2020Veraart et al, 2018;Chang et al, 2020;He et al, 2020;Kaupper et al, 2021). Here, such interactions expand the habitat range of the aerobic methanotrophs to encompass unexpected environments which usually do not meet the physiological requirements for aerobic methane oxidation.…”

Section: Aerobic Methanotrophs Under Micro-oxic Conditionsmentioning

confidence: 99%

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

et al. 2021

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Methane is the final product of the anaerobic decomposition of organic matter. The conversion of organic matter to methane (methanogenesis) as a mechanism for energy conservation is exclusively attributed to the archaeal domain. Methane is oxidized by methanotrophic microorganisms using oxygen or alternative terminal electron acceptors. Aerobic methanotrophic bacteria belong to the phyla Proteobacteria and Verrucomicrobia, while anaerobic methane oxidation is also mediated by more recently discovered anaerobic methanotrophs with representatives in both the bacteria and the archaea domains. The anaerobic oxidation of methane is coupled to the reduction of nitrate, nitrite, iron, manganese, sulfate, and organic electron acceptors (e.g., humic substances) as terminal electron acceptors. This review highlights the relevance of methanotrophy in natural and anthropogenically influenced ecosystems, emphasizing the environmental conditions, distribution, function, co-existence, interactions, and the availability of electron acceptors that likely play a key role in regulating their function. A systematic overview of key aspects of ecology, physiology, metabolism, and genomics is crucial to understand the contribution of methanotrophs in the mitigation of methane efflux to the atmosphere. We give significance to the processes under microaerophilic and anaerobic conditions for both aerobic and anaerobic methane oxidizers. In the context of anthropogenically influenced ecosystems, we emphasize the current and potential future applications of methanotrophs from two different angles, namely methane mitigation in wastewater treatment through the application of anaerobic methanotrophs, and the biotechnological applications of aerobic methanotrophs in resource recovery from methane waste streams. Finally, we identify knowledge gaps that may lead to opportunities to harness further the biotechnological benefits of methanotrophs in methane mitigation and for the production of valuable bioproducts enabling a bio-based and circular economy.

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Section: Aerobic Methanotrophs Under Micro-oxic Conditionsmentioning

confidence: 99%

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

et al. 2021

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“…S1). These concentrations were selected based on the effects of NH 4 Cl on the methane uptake rates in the same soil (i.e., dose-dependent inhibition of methane uptake was proportional to NH 4 Cl concentrations) (Ho et al 2020). All incubations (n = 3, each treatment) were performed in 120 ml bottles under 2-3% v/v methane in air at 27 °C while shaking (120 rpm) in the dark.…”

Section: Methodsmentioning

confidence: 99%

“…The pmoA gene sequences were deposited at the National Center for Biotechnology Information (NCBI) under the accession number PRJNA691142. The ammonium concentration was determined using standard colorimetric methods as described before (Ho et al 2020). Exchangeable ammonium, regarded as the total amount of ammonium present, was determined in 2 M KCl (1:2) after filtration (0.22 µm), whereas soluble ammonium was determined in the liquid phase of the soil slurry and enrichment, after centrifugation and filtration (0.22 µm).…”

Section: Methodsmentioning

confidence: 99%

“…The seemingly contradictory effects of ammonium on methane oxidation have been attributable to the dose and mineral forms of ammonium (e.g., ammonium chloride, ammonium sulfate) (Hu and Lu 2015;Krause et al 2012;Mohanty et al 2006;Walkiewicz et al 2018;Xu and Inubushi 2004), as well as the methane concentration (King and Schnell 1998). Besides edaphic properties controlling methane oxidation (Ho et al 2013a;Kaupper et al 2020b), the methanotrophs, as well as the non-methanotrophic members of the community, are relevant biotic determinants potentially affecting the response of methane oxidation to external stressors, e.g., high ammonium input (Ho et al 2020;Kaupper et al 2020c;2021;Mohanty et al 2006). With prior or continuous exposure to ammonium, an ammonium-tolerant methanotrophic community may emerge over time (Ho et al 2020;Qiu et al 2008).…”

Section: Introductionmentioning

confidence: 99%

“…Besides edaphic properties controlling methane oxidation (Ho et al 2013a;Kaupper et al 2020b), the methanotrophs, as well as the non-methanotrophic members of the community, are relevant biotic determinants potentially affecting the response of methane oxidation to external stressors, e.g., high ammonium input (Ho et al 2020;Kaupper et al 2020c;2021;Mohanty et al 2006). With prior or continuous exposure to ammonium, an ammonium-tolerant methanotrophic community may emerge over time (Ho et al 2020;Qiu et al 2008). Typically, the gammaproteobacterial methanotrophs (subgroup type Ia; Methylobacter, Methylomicrobium, Methylosarcina) are more responsive and show higher N assimilation, benefiting from short-term ammonium availability more than the alphaproteobacterial methanotrophs (subgroup type II; Methylocystis, Methylosinus) (Nold et al 1999;Noll et al 2008;Yang et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Discrepancy in exchangeable and soluble ammonium-induced effects on aerobic methane oxidation: a microcosm study of a paddy soil

et al. 2021

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Ammonium-induced stimulatory, inhibitory, and/or neutral effects on soil methane oxidation have been attributable to the ammonium concentration and mineral forms, confounded by other edaphic properties (e.g., pH, salinity), as well as the site-specific composition of the methanotrophic community. We hypothesize that this inconsistency may stem from the discrepancy in the cation adsorption capacity of the soil. We postulate that the effects of ammonium on the methanotrophic activity in soil are more accurately portrayed by relating methane uptake rates to the soluble ammonium (bioavailable), rather than the exchangeable (total) ammonium. To reduce adsorption (exchangeable) sites for ammonium in a paddy soil, two successive pre-incubation steps were introduced resulting in a 1000-fold soil dilution (soil enrichment), to be compared to a soil slurry (tenfold dilution) incubation. Ammonium was supplemented as NH4Cl at 0.5–4.75gL−1 after pre-incubation. While NH4Cl significantly stimulated the methanotrophic activity at all concentrations in the soil slurry incubation, methane uptake showed a dose-dependent effect in the soil enrichment. The trend in methane uptake could be explained by the soluble ammonium concentration, which was proportionate to the supplemented ammonium in the soil enrichment. In the soil slurry incubation, a fraction (36–63%) of the supplemented ammonium was determined to be adsorbed to the soil. Accordingly, Methylosarcina was found to predominate the methanotrophic community after the incubation, suggesting the relevance of this methanotroph at elevated ammonium levels (< 3.25gL−1 NH4Cl). Collectively, our results showed that the soluble, rather than the exchangeable ammonium concentration, is relevant when determining the effects of ammonium on methane oxidation, but this does not exclude other (a)biotic factors concurrently influencing methanotrophic activity.

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Aerobic Methanotrophy and Co-occurrence Networks of a Tropical Rainforest and Oil Palm Plantations in Malaysia

Zuan

Mendes

et al. 2021

Microb Ecol

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Oil palm (OP) plantations are gradually replacing tropical rainforest in Malaysia, one of the largest palm oil producers globally. Conversion of lands to OP plantations has been associated with compositional shifts of the microbial community, with consequences on the greenhouse gas (GHG) emissions. While the impact of the change in land use has recently been investigated for microorganisms involved in N2O emission, the response of the aerobic methanotrophs to OP agriculture remains to be determined. Here, we monitored the bacterial community composition, focusing on the aerobic methanotrophs, in OP agricultural soils since 2012, 2006, and 1993, as well as in a tropical rainforest, in 2019 and 2020. High-affinity methane uptake was confirmed, showing significantly lower rates in the OP plantations than in the tropical rainforest, but values increased with continuous OP agriculture. The bacterial, including the methanotrophic community composition, was modified with ongoing OP agriculture. The methanotrophic community composition was predominantly composed of unclassified methanotrophs, with the canonical (Methylocystis) and putative methanotrophs thought to catalyze high-affinity methane oxidation present at higher relative abundance in the oldest OP plantation. Results suggest that the methanotrophic community was relatively more stable within each site, exhibiting less temporal variations than the total bacterial community. Uncharacteristically, a 16S rRNA gene-based co-occurrence network analysis revealed a more complex and connected community in the OP agricultural soil, which may influence the resilience of the bacterial community to disturbances. Overall, we provide a first insight into the ecology and role of the aerobic methanotrophs as a methane sink in OP agricultural soils.

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Response of a methane-driven interaction network to stressor intensification

Cited by 21 publications

References 80 publications

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

Discrepancy in exchangeable and soluble ammonium-induced effects on aerobic methane oxidation: a microcosm study of a paddy soil

Aerobic Methanotrophy and Co-occurrence Networks of a Tropical Rainforest and Oil Palm Plantations in Malaysia

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