Methanol consumption drives the bacterial chloromethane sink in a forest soil

Pauline Chaignaud,Françoise Bringel,Ludovic Besaury,Mareen Morawe,Stéphane Vuilleumier,Eileen Kröber,Steffen Kolb

doi:10.1038/s41396-018-0228-4

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.

Highlights

Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.Chloromethane (CH3Cl) is the most abundant halogenated volatile organic compound (VOC) in the atmosphere and contributes substantially to destruction of stratospheric ozone [1, 2]
The reverse combined amendment of unlabeled CH3Cl degraders also grow with methanol (CH3OH) with [13C]-CH3Cl led to increased mineralization of [13C]-CH3Cl (Fig. S1). These findings suggest that activity and growth of soil microorganisms that define the bacterial CH3Cl sink in the investigated soil strongly depend on availability of CH3OH
Our study provides a first deep coverage exploration of bacterial diversity functionally linked with the CH3Cl sink in soil

Summary

Introduction

Global emissions reach about 2.0 ± 0.6 Tg CH3Cl per year [3, 4]. Current knowledge suggests that terrestrial CH3Cl emissions are mainly associated with biological activities of the aboveground part of plants and with white rot fungi in soil [5,6,7]. CH3Cl is produced upon burning of plant biomass, from methoxy groups of plant structural components such as lignin and pectin [8, 9]. CH3Cl is enzymatically produced by S-adenosylmethionine-dependent methylation of chloride [10]. Current estimates for the global sink are larger than the global source [3], to which forest soil could contribute as much as 1.0 Tg per year [3, 11]. Global budgets are still uncertain, as the nature of the biotic sink activity as well as its spatial and temporal variability are not known at the regional and global scale [12]

Methods

Results

Discussion

Conclusion