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Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes.

ABSTRACT: Methane (CH(4)) flux to the atmosphere is mitigated via microbial CH(4) oxidation in sediments and water. As arctic temperatures increase, understanding the effects of temperature on the activity and identity of methanotrophs in arctic lake sediments is important to predicting future CH(4) emissions. We used DNA-based stable-isotope probing (SIP), quantitative PCR (Q-PCR), and pyrosequencing analyses to identify and characterize methanotrophic communities active at a range of temperatures (4°C, 10°C, and 21°C) in sediments (to a depth of 25 cm) sampled from Lake Qalluuraq on the North Slope of Alaska. CH(4) oxidation activity was measured in microcosm incubations containing sediments at all temperatures, with the highest CH(4) oxidation potential of 37.5 ?mol g(-1) day(-1) in the uppermost (depth, 0 to 1 cm) sediment at 21°C after 2 to 5 days of incubation. Q-PCR of pmoA and of the 16S rRNA genes of type I and type II methanotrophs, and pyrosequencing of 16S rRNA genes in (13)C-labeled DNA obtained by SIP demonstrated that the type I methanotrophs Methylobacter, Methylomonas, and Methylosoma dominated carbon acquisition from CH(4) in the sediments. The identity and relative abundance of active methanotrophs differed with the incubation temperature. Methylotrophs were also abundant in the microbial community that derived carbon from CH(4), especially in the deeper sediments (depth, 15 to 20 cm) at low temperatures (4°C and 10°C), and showed a good linear relationship (R = 0.82) with the relative abundances of methanotrophs in pyrosequencing reads. This study describes for the first time how methanotrophic communities in arctic lake sediments respond to temperature variations.

SUBMITTER: He R

PROVIDER: S-EPMC3370501 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes.

He Ruo R Wooller Matthew J MJ Pohlman John W JW Quensen John J Tiedje James M JM Leigh Mary Beth MB

Applied and environmental microbiology 20120420 13

Methane (CH(4)) flux to the atmosphere is mitigated via microbial CH(4) oxidation in sediments and water. As arctic temperatures increase, understanding the effects of temperature on the activity and identity of methanotrophs in arctic lake sediments is important to predicting future CH(4) emissions. We used DNA-based stable-isotope probing (SIP), quantitative PCR (Q-PCR), and pyrosequencing analyses to identify and characterize methanotrophic communities active at a range of temperatures (4°C, ...[more]

PMID: 22522690

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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:Although cold environments are major contributors to global biogeochemical cycles, comparatively little is known about their microbial community function, structure, and limits of activity. In this study a microcosm based approach was used to investigate the effects of temperature, and methanogenic substrate amendment, (acetate, methanol and H2/CO2) on methanogen activity and methanogen community structure in high Arctic wetlands (Solvatnet and Stuphallet, Svalbard). Methane production was not detected in Stuphallet sediment microcosms (over a 150 day period) and occurred within Solvatnet sediments microcosms (within 24 hours) at temperatures from 5 to 40°C, the maximum temperature being at far higher than in situ maximum temperatures (which range from air temperatures of -1.4 to 14.1°C during summer months). Distinct responses were observed in the Solvatnet methanogen community under different short term incubation conditions. Specifically, different communities were selected at higher and lower temperatures. At lower temperatures (5°C) addition of exogenous substrates (acetate, methanol or H2/CO2) had no stimulatory effect on the rate of methanogenesis or on methanogen community structure. The community in these incubations was dominated by members of the Methanoregulaceae/WCHA2-08 family-level group, which were most similar to the psychrotolerant hydrogenotrophic methanogen Methanosphaerula palustris strain E1-9c. In contrast, at higher temperatures, substrate amendment enhanced methane production in H2/CO2 amended microcosms, and played a clear role in structuring methanogen communities. Specifically, at 30°C members of the Methanoregulaceae/WCHA2-08 predominated following incubation with H2/CO2, and Methanosarcinaceaeand Methanosaetaceae were enriched in response to acetate addition. These results may indicate that in transiently cold environments, methanogen communities can rapidly respond to moderate short term increases in temperature, but not necessarily to the seasonal release of previously frozen organic carbon from thawing permafrost soils. However, as temperatures increase such inputs of carbon will likely have a greater influence on methane production and methanogen community structure. Understanding the action and limitations of anaerobic microorganisms within cold environments may provide information which can be used in defining region-specific differences in the microbial processes; which ultimately control methane flux to the atmosphere.

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Dataset Information

Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes.

Publications

Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes.

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