Dataset Information

Methanol consumption drives the bacterial chloromethane sink in a forest soil.

ABSTRACT: Halogenated volatile organic compounds (VOCs) emitted by terrestrial ecosystems, such as chloromethane (CH3Cl), have pronounced effects on troposphere and stratosphere chemistry and climate. The magnitude of the global CH3Cl sink is uncertain since it involves a largely uncharacterized microbial sink. CH3Cl represents a growth substrate for some specialized methylotrophs, while methanol (CH3OH), formed in much larger amounts in terrestrial environments, may be more widely used by such microorganisms. Direct measurements of CH3Cl degradation rates in two field campaigns and in microcosms allowed the identification of top soil horizons (i.e., organic plus mineral A horizon) as the major biotic sink in a deciduous forest. Metabolically active members of Alphaproteobacteria and Actinobacteria were identified by taxonomic and functional gene biomarkers following stable isotope labeling (SIP) of microcosms with CH3Cl and CH3OH, added alone or together as the [13C]-isotopologue. Well-studied reference CH3Cl degraders, such as Methylobacterium extorquens CM4, were not involved in the sink activity of the studied soil. Nonetheless, only sequences of the cmuA chloromethane dehalogenase gene highly similar to those of known strains were detected, suggesting the relevance of horizontal gene transfer for CH3Cl degradation in forest soil. Further, CH3Cl consumption rate increased in the presence of CH3OH. Members of Alphaproteobacteria and Actinobacteria were also 13C-labeled upon [13C]-CH3OH amendment. These findings suggest that key bacterial CH3Cl degraders in forest soil benefit from CH3OH as an alternative substrate. For soil CH3Cl-utilizing methylotrophs, utilization of several one-carbon compounds may represent a competitive advantage over heterotrophs that cannot utilize one-carbon compounds.

SUBMITTER: Chaignaud P

PROVIDER: S-EPMC6194010 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Methanol consumption drives the bacterial chloromethane sink in a forest soil.

Chaignaud Pauline P Morawe Mareen M Besaury Ludovic L Kröber Eileen E Vuilleumier Stéphane S Bringel Françoise F Kolb Steffen S

The ISME journal 20180710 11

Halogenated volatile organic compounds (VOCs) emitted by terrestrial ecosystems, such as chloromethane (CH3Cl), have pronounced effects on troposphere and stratosphere chemistry and climate. The magnitude of the global CH3Cl sink is uncertain since it involves a largely uncharacterized microbial sink. CH3Cl represents a growth substrate for some specialized methylotrophs, while methanol (CH3OH), formed in much larger amounts in terrestrial environments ...[more]

PMID: 29991765

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Project description:Methanol is an abundant atmospheric volatile organic compound that is released from both living and decaying plant material. In forest and other aerated soils, methanol can be consumed by methanol-utilizing microorganisms that constitute a known terrestrial sink. However, the environmental factors that drive the biodiversity of such methanol-utilizers have been hardly resolved. Soil-derived isolates of methanol-utilizers can also often assimilate multicarbon compounds as alternative substrates. Here, we conducted a comparative DNA stable isotope probing experiment under methylotrophic (only [13C1]-methanol was supplemented) and combined substrate conditions ([12C1]-methanol and alternative multi-carbon [13Cu]-substrates were simultaneously supplemented) to (i) identify methanol-utilizing microorganisms of a deciduous forest soil (European beech dominated temperate forest in Germany), (ii) assess their substrate range in the soil environment, and (iii) evaluate their trophic links to other soil microorganisms. The applied multi-carbon substrates represented typical intermediates of organic matter degradation, such as acetate, plant-derived sugars (xylose and glucose), and a lignin-derived aromatic compound (vanillic acid). An experimentally induced pH shift was associated with substantial changes of the diversity of active methanol-utilizers suggesting that soil pH was a niche-defining factor of these microorganisms. The main bacterial methanol-utilizers were members of the Beijerinckiaceae (Bacteria) that played a central role in a detected methanol-based food web. A clear preference for methanol or multi-carbon substrates as carbon source of different Beijerinckiaceae-affiliated phylotypes was observed suggesting a restricted substrate range of the methylotrophic representatives. Apart from Bacteria, we also identified the yeasts Cryptococcus and Trichosporon as methanol-derived carbon-utilizing fungi suggesting that further research is needed to exclude or prove methylotrophy of these fungi.

Project description:Summer droughts strongly affect soil organic carbon (SOC) cycling, but net effects on SOC storage are unclear as drought affects both C inputs and outputs from soils. Here, we explored the overlooked role of soil fauna on SOC storage in forests, hypothesizing that soil faunal activity is particularly drought-sensitive, thereby reducing litter incorporation into the mineral soil and, eventually, long-term SOC storage. In a drought-prone pine forest (Switzerland), we performed a large-scale irrigation experiment for 17 years and assessed its impact on vertical SOC distribution and composition. We also examined litter mass loss of dominant tree species using different mesh-size litterbags and determined soil fauna abundance and community composition. The 17-year-long irrigation resulted in a C loss in the organic layers (-1.0 kg C m-2 ) and a comparable C gain in the mineral soil (+0.8 kg C m-2 ) and thus did not affect total SOC stocks. Irrigation increased the mass loss of Quercus pubescens and Viburnum lantana leaf litter, with greater effect sizes when meso- and macrofauna were included (+215%) than when excluded (+44%). The enhanced faunal-mediated litter mass loss was paralleled by a many-fold increase in the abundance of meso- and macrofauna during irrigation. Moreover, Acari and Collembola community composition shifted, with a higher presence of drought-sensitive species in irrigated soils. In comparison, microbial SOC mineralization was less sensitive to soil moisture. Our results suggest that the vertical redistribution of SOC with irrigation was mainly driven by faunal-mediated litter incorporation, together with increased root C inputs. Our study shows that soil fauna is highly sensitive to natural drought, which leads to a reduced C transfer from organic layers to the mineral soil. In the longer term, this potentially affects SOC storage and, therefore, soil fauna plays a key but so far largely overlooked role in shaping SOC responses to drought.

Dataset Information

Methanol consumption drives the bacterial chloromethane sink in a forest soil.

Publications

Methanol consumption drives the bacterial chloromethane sink in a forest soil.

Similar Datasets

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