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.

Ecological Functions of Agricultural Soil Bacteria and Microeukaryotes in Chitin Degradation: A Case Study

“…To minimize sequencing effort and costs for the chitin substrate, our experiment was duplicated and SIP gradients were done from pooled RNA from both duplicates per time point and oxygen treatment. Previous studies revealed low technical variability (Morawe et al, 2017; Chaignaud et al, 2018). All labeled OTUs occurred at two or more time points.…”

Novel bacterial chloromethane degraders of a living tree fern evidenced by 13C-chloromethane incubations

“…Labelled OTUs were defined according to four criteria (adapted from [41] (https://mage.genoscope.cns.fr/microscope/mage/). In addition, BLAST [73] and RAST [78] were used to further compare MAG genetic content and assess potentials for CH3Cl utilization by screening for functional marker genes involved in CH3Cl utilization, one-carbon metabolism, central metabolism, co-factor synthesis, transport systems, and stress response.…”

“…The cmu pathway is the only characterized pathway for utilisation of CH3Cl [35]. Of the cmuAand cmuB-encoded methyltransferases of chloromethane dehalogenase, the cmuA gene is the most conserved and has been frequently used as the cmu pathway gene marker [109]. CmuA (data not shown) when using shortBRED.…”

Transcriptional regulation of organohalide pollutant utilisation in bacteria

“…In this context, laboratory microcosms using environmental samples of water, sediment and soil have increasingly been developed to study bacterial dehalogenation. Such microcosms provide conditions mimicking in situ environmental conditions, while allowing for controlled growth conditions and monitoring (Amos et al 2008;Chaignaud et al 2018;Lillis, Clipson and Doyle 2010;Xiu et al 2010;Men et al 2017). For example, pollutant degradation could be quantitatively correlated with transcription of dehalogenase gene cbdbA in water microcosms exposed to hexachlorobenzene at several temperatures (Tas et al 2011).…”

“…For example, pollutant degradation could be quantitatively correlated with transcription of dehalogenase gene cbdbA in water microcosms exposed to hexachlorobenzene at several temperatures (Tas et al 2011). Microcosms also enabled investigations of bacterial dehalogenation in the context of microbial interactions with other types of organisms such as plants (Liu et al 2007;Scheublin et al 2014;Chaignaud et al 2018;Wang et al 2018). Such studies are likely to continue to develop in the future, and to allow improved assessment of environmentally relevant processes, such as the fate of plant-emitted chlorinated C 1 volatile organic compounds and their consumption by dehalogenating methylotrophs (reviewed in Couée 2015, Bringel et al, 2019).…”