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Methylotrophs and Methylotroph Populations for Chloromethane Degradation Françoise Bringel1*, Ludovic Besaury2, Pierre Amato3, Eileen Kröber4, Stefen Kolb4, Frank Keppler5,6, Stéphane Vuilleumier1 and Thierry Nadalig1 1Université de Strasbourg UMR 7156 UNISTR CNRS, Molecular Genetics, Genomics, Microbiology (GMGM), Strasbourg, France. 2Université de Reims Champagne-Ardenne, Chaire AFERE, INR, FARE UMR A614, Reims, France. 3 Université Clermont Auvergne, CNRS, SIGMA Clermont, ICCF, Clermont-Ferrand, France. 4Microbial Biogeochemistry, Research Area Landscape Functioning – Leibniz Centre for Agricultural Landscape Research – ZALF, Müncheberg, Germany. 5Institute of Earth Sciences, Heidelberg University, Heidelberg, Germany. 6Heidelberg Center for the Environment HCE, Heidelberg University, Heidelberg, Germany. *Correspondence: [email protected] htps://doi.org/10.21775/cimb.033.149 Abstract characterized ‘chloromethane utilization’ (cmu) Chloromethane is a halogenated volatile organic pathway, so far. Tis pathway may not be representa- compound, produced in large quantities by terres- tive of chloromethane-utilizing populations in the trial vegetation. Afer its release to the troposphere environment as cmu genes are rare in metagenomes. and transport to the stratosphere, its photolysis con- Recently, combined ‘omics’ biological approaches tributes to the degradation of stratospheric ozone. A with chloromethane carbon and hydrogen stable beter knowledge of chloromethane sources (pro- isotope fractionation measurements in microcosms, duction) and sinks (degradation) is a prerequisite indicated that microorganisms in soils and the phyl- to estimate its atmospheric budget in the context of losphere (plant aerial parts) represent major sinks global warming. Te degradation of chloromethane of chloromethane in contrast to more recently by methylotrophic communities in terrestrial envi- recognized microbe-inhabited environments, such ronments is a major underestimated chloromethane as clouds. Cultivated chloromethane-degraders sink. Methylotrophs isolated from soils, marine envi- lacking cmu genes display a singular isotope frac- ronments and more recently from the phyllosphere tionation signature of chloromethane. Moreover, 13 have been grown under laboratory conditions using CH3Cl labelling of active methylotrophic commu- chloromethane as the sole carbon source. In addi- nities by stable isotope probing in soils identify taxa tion to anaerobes that degrade chloromethane, that difer from those known for chloromethane the majority of cultivated strains were isolated in degradation. Tese observations suggest that new aerobiosis for their ability to use chloromethane biomarkers for detecting active microbial chlo- as sole carbon and energy source. Among those, romethane-utilizers in the environment are needed the Proteobacterium Methylobacterium (recently to assess the contribution of microorganisms to the reclassifed as Methylorubrum) harbours the only global chloromethane cycle. Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb 150 | Bringel et al. Introduction much more efcient at higher temperatures such as those reached during pyrolysis and biomass Chloromethane and stratospheric burning (Hamilton et al., 2003; Keppler, 2005; ozone depletion McRoberts et al., 2015). Chloromethane release Chloromethane (methyl chloride, CH3Cl) is was also detected during thermal conversion of the most abundant organohalogen in the Earth Martian soils by the Mars landers Viking (Bie- atmosphere. Its global production is estimated mann et al., 1976) and Curiosity (Ming et al., at 4–5 megatons per year, with main sources 2014), indicating the presence of endogenous stemming from terrestrial vegetation (Keppler, organic mater on Mars. Chloromethane emis- 2005). Photolytic degradation of chloromethane sion profles during thermal treatment of soils releases a halogen radical, which catalyses the sampled from other hyperarid environments destruction of ozone. Tus, chloromethane con- hostile microbial life such as the Atacama desert tributes to depletion of the stratospheric ozone were almost identical to those recorded by the layer (altitude of approximately 20 to 30 km), Curiosity rover on Mars (Schulze-Makuch et which constitutes the Earth’s natural protective al., 2018). Furthermore, chloromethane forma- shield that absorbs the solar UVC and partially tion was observed from thermal conversion of UVB radiation dangerous for living organisms. extraterrestrial material such as carbonaceous Until the 1990s, chloromethane was used as meteorites (Keppler et al., 2014) and in protos- a refrigerant under the name Freon 40. Chlo- tellar environments (Fayolle et al., 2017). Tese romethane has a stratospheric lifetime of about recent observations contributed to the emer- one year, much shorter than most other chloro- gence of an ‘astronomical’ fundamental interest fuorocarbons (CFCs), solvents and halons also in the understanding of chloromethane’s cycle in banned by the international agreement of 1987 sun-like stars and on Earth. known as the Montreal Protocol on substances On Earth, plants (alive or decaying) are a that deplete the ozone layer (see web resource major biotic source of chloromethane. Chlo- section). Tere are still some uncertainties about romethane is produced by enzymatic chloride ion chloromethane anthropogenic emissions (e.g. coal methylation, as shown in higher plants afliated combustion, feedstock for chemical industries) to the Brassicaceae family (Atieh et al., 1995; (Li et al., 2017). Chloromethane is responsible Rhew et al., 2003) and wood-degrading fungi alone for approximately 16% of stratospheric (Harper et al., 1990). Te S-adenosyl-l-methio- chlorine-catalysed ozone destruction (Carpenter nine-dependent halide ion methyltransferase is et al., 2014). A detailed understanding of its encoded by gene HOL1 (Harmless to Ozone sources and sinks will be essential to predict Layer) in Arabidopsis thaliana (Nagatoshi and changes in atmospheric chloromethane fuxes in Nakamura, 2009). HOL1 gene disruption corre- the context of global climate change. lates with decreased pathogen defence, possibly due to reduced production of methyl thiocy- Chloromethane sources and sinks anate (CH3SCN) from glucosinolate-derived Chloromethane formation in plants and soil thiocyanate by HOL1 (Manley, 2002; Rhew involves biotic and abiotic processes. Chloride et al., 2003; Nagatoshi and Nakamura, 2009). ion can be alkylated during the abiotic oxida- Chloromethane production is considered a by- tion of organic mater by an electron acceptor product of plant thiocyanate metabolism. Such such as Fe(III) in soils and sediments (Kep- methyltransferases have also been detected in pler et al., 2000). Abiotic chloromethane mainly other crop and seaside plants (Itoh et al., 2009) results from the conversion of plant methoxyl including marine algae (Wuosmaa and Hager, groups (ether- or ester-bonded methyl groups) 1990; Ohsawa et al., 2001; Toda and Itoh, 2011). and their reaction with chloride ion (Keppler et Identifed chloromethane sinks are dominated al., 2000; Hamilton et al., 2003; Sailaukhanuly by abiotic loss processes in the atmosphere et al., 2014). Tis process occurs in terrestrial involving reaction with OH radicals, or via ecosystems at ambient temperatures (Derendorp chlorine radicals in the marine atmospheric et al., 2012; Keppler et al., 2014), but it is boundary layer (see Web resources). Te extent Bacterial Chloromethane Degradation | 151 of consumption of chloromethane under the possibility raises questions about the composi- control of biological processes, especially by tion, distribution, functioning and evolution of microorganisms, constitutes one of the largest chloromethane-utilizing populations in response uncertainties regarding the global budget of chlo- to highly fuctuating emissions of this volatile romethane (Harper and Hamilton, 2003; Keppler, halogenated compound at the soil-plant-atmos- 2005). phere interfaces. Microbial degradation: an underestimated sink in the global Assessing bacterial chloromethane budget chloromethane sinks Te study of ecology and diversity of chlo- Recent investigations of plant and soil samples romethane and other methyl halide-degrading suggest that chloromethane-degraders represent a microorganisms remain a challenging feld of minor fraction of microbial communities (Chaig- environmental biology. Key microbial enzymes naud et al., 2018; Jaeger et al., 2018a,b) that are of (de)halogenation activity and active microor- estimated as 107 cells per cm2 of leaf surface ganisms in chlorine and other halogens (fuorine, to 109 cells per g of soil (Vorholt, 2012). In bromine, iodine) cycling remain largely unknown air, microbial concentrations range from a few (Weigold et al., 2016). Te global impact of tens to billions per cubic metre depending on microorganisms on the chloromethane sink is location, altitude above ground, and time of the difcult to quantify due to concomitant processes day and year (Amato et al., 2017a; DasSarma of production and degradation of chloromethane and DasSarma, 2018), representing a total of in the environment. For instance, highly fuctuat- 1019 bacterial cells in the atmosphere (Whitman ing chloromethane emissions occur in fern plants et al., 1998). Microorganisms collected from as recently discussed (Jaeger et al., 2018b). Both aerosols, cloud and rain waters retain metabolic production and degradation of chloromethane activity under cloud-like conditions and are may coexist

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