Methylotrophs and methylotroph populations for chloromethane degradation Françoise Bringel, Ludovic Besaury, Pierre Amato, Eileen Kröber, Steffen Kolb, Frank Keppler, Stéphane Vuilleumier, Thierry Nadalig To cite this version: Françoise Bringel, Ludovic Besaury, Pierre Amato, Eileen Kröber, Steffen Kolb, et al.. Methylotrophs and methylotroph populations for chloromethane degradation. Ludmila Chistoserdova. Methy- lotrophs and methylotroph communities, Caister Academic Press, pp.149-172, 2019, 978-1-912530- 19-9. 10.21775/cimb.033.149. hal-02350630 HAL Id: hal-02350630 https://hal.archives-ouvertes.fr/hal-02350630 Submitted on 6 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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Methylotrophs and Methylotroph Populations for Chloromethane Degradation 8 Françoise Bringel1*, Ludovic Besaury2, Pierre Amato3, Eileen Kröber4, Steffen Kolb4, Frank Keppler5,6, Stéphane Vuilleumier1 and Thierry Nadalig1 1Université de Strasbourg UMR 7156 UNISTRA CNRS, Molecular Genetics, Genomics, Microbiology (GMGM), Strasbourg, France. 2Université de Reims Champagne-Ardenne, Chaire AFERE, INRA, 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] https://doi.org/10.21775/9781912530045.08 Abstract characterized ‘chloromethane utilization’ (cmu) Chloromethane is a halogenated volatile organic pathway, so far. This pathway may not be representa- compound, produced in large quantities by terres- tive of chloromethane-utilizing populations in the trial vegetation. After 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 better 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. The 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 differ from those known for chloromethane the majority of cultivated strains were isolated in degradation. These 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 reclassified as Methylorubrum) harbours the only global chloromethane cycle. Date: 12:26 Friday 15 March 2019 UNCORRECTED PROOF File: Methylotrophs 3P 150 | Bringel et al. Introduction much more efficient 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 matter on Mars. Chloromethane emis- 2005). Photolytic degradation of chloromethane sion profiles during thermal treatment of soils releases a halogen radical, which catalyses the sampled from other hyperarid environments destruction of ozone. Thus, 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). These 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 fluorocarbons (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). There are still some uncertainties about romethane is produced by enzymatic chloride ion chloromethane anthropogenic emissions (e.g. coal methylation, as shown in higher plants affiliated combustion, feedstock for chemical industries) to the Brassicaceae family (Attieh 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). The 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 fluxes 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 matter 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 Identified chloromethane sinks are dominated al., 2000; Hamilton et al., 2003; Sailaukhanuly by abiotic loss processes in the atmosphere et al., 2014). This 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 resource section). The Date: 12:26 Friday 15 March 2019 UNCORRECTED PROOF File: Methylotrophs 3P Bacterial Chloromethane Degradation | 151 extent of consumption of chloromethane under possibility raises questions about the composi- the 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 fluctuating 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 The study of ecology and diversity of chlo- Recent investigations of plant and soil samples