Dataset Information

Resilience of aerobic methanotrophs in soils; spotlight on the methane sink under agriculture.

ABSTRACT: Aerobic methanotrophs are a specialized microbial group, catalyzing the oxidation of methane. Disturbance-induced loss of methanotroph diversity/abundance, thus results in the loss of this biological methane sink. Here, we synthesized and conceptualized the resilience of the methanotrophs to sporadic, recurring, and compounded disturbances in soils. The methanotrophs showed remarkable resilience to sporadic disturbances, recovering in activity and population size. However, activity was severely compromised when disturbance persisted or reoccurred at increasing frequency, and was significantly impaired following change in land use. Next, we consolidated the impact of agricultural practices after land conversion on the soil methane sink. The effects of key interventions (tillage, organic matter input, and cover cropping) where much knowledge has been gathered were considered. Pairwise comparisons of these interventions to nontreated agricultural soils indicate that the agriculture-induced impact on the methane sink depends on the cropping system, which can be associated to the physiology of the methanotrophs. The impact of agriculture is more evident in upland soils, where the methanotrophs play a more prominent role than the methanogens in modulating overall methane flux. Although resilient to sporadic disturbances, the methanotrophs are vulnerable to compounded disturbances induced by anthropogenic activities, significantly affecting the methane sink function.

SUBMITTER: Lim J

PROVIDER: S-EPMC10872700 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Resilience of aerobic methanotrophs in soils; spotlight on the methane sink under agriculture.

Lim Jiyeon J Wehmeyer Helena H Heffner Tanja T Aeppli Meret M Gu Wenyu W Kim Pil Joo PJ Horn Marcus A MA Ho Adrian A

FEMS microbiology ecology 20240201 3

Aerobic methanotrophs are a specialized microbial group, catalyzing the oxidation of methane. Disturbance-induced loss of methanotroph diversity/abundance, thus results in the loss of this biological methane sink. Here, we synthesized and conceptualized the resilience of the methanotrophs to sporadic, recurring, and compounded disturbances in soils. The methanotrophs showed remarkable resilience to sporadic disturbances, recovering in activity and population size. However, activity was severely ...[more]

PMID: 38327184

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Project description:BackgroundMicrobial methane oxidation, methanotrophy, plays a crucial role in mitigating the release of the potent greenhouse gas methane from aquatic systems. While aerobic methanotrophy is a well-established process in oxygen-rich environments, emerging evidence suggests their activity in hypoxic conditions. However, the adaptability of these methanotrophs to such environments has remained poorly understood. Here, we explored the genetic adaptability of aerobic methanotrophs to hypoxia in the methanogenic sediments of Lake Kinneret (LK). These LK methanogenic sediments, situated below the oxidic and sulfidic zones, were previously characterized by methane oxidation coupled with iron reduction via the involvement of aerobic methanotrophs.ResultsIn order to explore the adaptation of the methanotrophs to hypoxia, we conducted two experiments using LK sediments as inoculum: (i) an aerobic "classical" methanotrophic enrichment with ambient air employing DNA stable isotope probing (DNA-SIP) and (ii) hypoxic methanotrophic enrichment with repeated spiking of 1% oxygen. Analysis of 16S rRNA gene amplicons revealed the enrichment of Methylococcales methanotrophs, being up to a third of the enriched community. Methylobacter, Methylogaea, and Methylomonas were prominent in the aerobic experiment, while hypoxic conditions enriched primarily Methylomonas. Using metagenomics sequencing of DNA extracted from these experiments, we curated five Methylococcales metagenome-assembled genomes (MAGs) and evaluated the genetic basis for their survival in hypoxic environments. A comparative analysis with an additional 62 Methylococcales genomes from various environments highlighted several core genetic adaptations to hypoxia found in most examined Methylococcales genomes, including high-affinity cytochrome oxidases, oxygen-binding proteins, fermentation-based methane oxidation, motility, and glycogen use. We also found that some Methylococcales, including LK Methylococcales, may denitrify, while metals and humic substances may also serve as electron acceptors alternative to oxygen. Outer membrane multi-heme cytochromes and riboflavin were identified as potential mediators for the utilization of metals and humic material. These diverse mechanisms suggest the ability of methanotrophs to thrive in ecological niches previously thought inhospitable for their growth.ConclusionsOur study sheds light on the ability of enriched Methylococcales methanotrophs from methanogenic LK sediments to survive under hypoxia. Genomic analysis revealed a spectrum of genetic capabilities, potentially enabling these methanotrophs to function. The identified mechanisms, such as those enabling the use of alternative electron acceptors, expand our understanding of methanotroph resilience in diverse ecological settings. These findings contribute to the broader knowledge of microbial methane oxidation and have implications for understanding and potential contribution methanotrophs may have in mitigating methane emissions in various environmental conditions.

Project description:Non-microbial methane (NM-CH4), emissions from soil might play a significant role in carbon cycling and global climate change. However, the production mechanisms and emission potential of soil NM-CH4 from tropical rainforest remain highly uncertain. In order to explore the laws and characteristics of NM-CH4 emission from tropical rainforest soils. Incubation experiments at different environmental conditions (temperatures, soil water contents, hydrogen peroxide) and for soils with different soil organic carbon (SOC) contents were conducted to investigate the NM-CH4 emission characteristics and its influence factors of soils (0-10cm) that collected from a tropical rainforest in Hainan, China. Incubation results illustrated that soil NM-CH4 release showed a linear increase with the incubation time in the first 24 hours at 70 °C, whereas the logarithmic curve increase was found in 192 h incubation. Soil NM-CH4 emission rates under aerobic condition were significantly higher than that of under anaerobic condition at first 24 h incubation. The increasing of temperature, suitable soil water contents (0-100%), and hydrogen peroxide significantly promoted soil NM-CH4 emission rates at the first 24 h incubation. However, excessive soil water contents (200%) inhibited soil NM-CH4 emissions. According to the curve simulated from the NM-CH4 emission rates and incubation time at 70 °C of aerobic condition, soil would no longer release NM-CH4 after 229 h incubation. The NM-CH4 emissions were positively corelated with SOC contents, and the average soil NM-CH4 emission potential was about 6.91 ug per gram organic carbon in the tropical mountain rainforest. This study revealed that soils in the tropical rainforest could produce NM-CH4 under certain environment conditions and it supported production mechanisms of thermal degradation and reactive oxygen species oxidation. Those results could provide a basic data for understanding the soil NM-CH4 production mechanisms and its potential in the tropical rainforest.

Dataset Information

Resilience of aerobic methanotrophs in soils; spotlight on the methane sink under agriculture.

Publications

Resilience of aerobic methanotrophs in soils; spotlight on the methane sink under agriculture.

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