Chloride‐associated adaptive response in aerobic methylotrophic dichloromethane‐utilising bacteria

Torgonskaya, M. L.; Доронина, Н. В.; Hourcade, Édith; Trotsenko, Yu. A.; Vuilleumier, Stéphane

doi:10.1002/jobm.201000280

Cited by 18 publications

(7 citation statements)

References 29 publications

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“…Some methylotrophic microorganisms are able to utilize chlorinated methanes (such as CM and DCM) as their sole carbon and energy source for growth (Muller et al, 2011a ; Nadalig et al, 2014 ). Bacterial CM and DCM utilization starts with dehalogenation, causing diverse physiological stresses such as production of intracellular HCl, which lowers pH and increases ionic strength, and formation of DNA adducts (Kayser and Vuilleumier, 2001 ; Torgonskaya et al, 2011 ; Michener et al, 2014b , 2016 ). The mechanisms allowing methylotrophic bacteria to cope with dehalogenation-induced stress are still poorly understood, despite potential use of such bacteria for bioremediation.…”

Section: Introductionmentioning

confidence: 99%

Genomic and Transcriptomic Analysis of Growth-Supporting Dehalogenation of Chlorinated Methanes in Methylobacterium

et al. 2017

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Bacterial adaptation to growth with toxic halogenated chemicals was explored in the context of methylotrophic metabolism of Methylobacterium extorquens, by comparing strains CM4 and DM4, which show robust growth with chloromethane and dichloromethane, respectively. Dehalogenation of chlorinated methanes initiates growth-supporting degradation, with intracellular release of protons and chloride ions in both cases. The core, variable and strain-specific genomes of strains CM4 and DM4 were defined by comparison with genomes of non-dechlorinating strains. In terms of gene content, adaptation toward dehalogenation appears limited, strains CM4 and DM4 sharing between 75 and 85% of their genome with other strains of M. extorquens. Transcript abundance in cultures of strain CM4 grown with chloromethane and of strain DM4 grown with dichloromethane was compared to growth with methanol as a reference C1 growth substrate. Previously identified strain-specific dehalogenase-encoding genes were the most transcribed with chlorinated methanes, alongside other genes encoded by genomic islands (GEIs) and plasmids involved in growth with chlorinated compounds as carbon and energy source. None of the 163 genes shared by strains CM4 and DM4 but not by other strains of M. extorquens showed higher transcript abundance in cells grown with chlorinated methanes. Among the several thousand genes of the M. extorquens core genome, 12 genes were only differentially abundant in either strain CM4 or strain DM4. Of these, 2 genes of known function were detected, for the membrane-bound proton translocating pyrophosphatase HppA and the housekeeping molecular chaperone protein DegP. This indicates that the adaptive response common to chloromethane and dichloromethane is limited at the transcriptional level, and involves aspects of the general stress response as well as of a dehalogenation-specific response to intracellular hydrochloric acid production. Core genes only differentially abundant in either strain CM4 or strain DM4 total 13 and 58 CDS, respectively. Taken together, the obtained results suggest different transcriptional responses of chloromethane- and dichloromethane-degrading M. extorquens strains to dehalogenative metabolism, and substrate- and pathway-specific modes of growth optimization with chlorinated methanes.

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Section: Introductionmentioning

confidence: 99%

Genomic and Transcriptomic Analysis of Growth-Supporting Dehalogenation of Chlorinated Methanes in Methylobacterium

et al. 2017

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“…This strain is the best‐studied DCM‐degrading isolate. Its genome was fully sequenced (Vuilleumier et al ., 2009), and several studies have documented the effects of DCM degradation by its DCM dehalogenase DcmA on cellular metabolism (Gisi et al ., 1998; 1999; Evans et al ., 2000; Kayser et al ., 2000; Kayser and Vuilleumier, 2001; Torgonskaya et al ., 2011). Bacteria of the genus Methylobacterium are pink‐pigmented facultative methylotrophs which grow with reduced organic compounds without carbon–carbon bonds such as methanol, and with multi‐carbon compounds such as succinate, pyruvate, acetate and ethanol.…”

Section: Introductionmentioning

confidence: 99%

Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4

Muller

Hourcade

Louhichi-Jelail

et al. 2011

Environmental Microbiology

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Dichloromethane (CH(2)Cl(2) , DCM) is a chlorinated solvent mainly produced by industry, and a common pollutant. Some aerobic methylotrophic bacteria are able to grow with this chlorinated methane as their sole carbon and energy source, using a DCM dehalogenase/glutathione S-transferase encoded by dcmA to transform DCM into two molecules of HCl and one molecule of formaldehyde, a toxic intermediate of methylotrophic metabolism. In Methylobacterium extorquens DM4 of known genome sequence, dcmA lies on a 126 kb dcm genomic island not found so far in other DCM-dechlorinating strains. An experimental search for the molecular determinants involved in specific cellular responses of strain DM4 growing with DCM was performed. Random mutagenesis with a minitransposon containing a promoterless reporter gfp gene yielded 25 dcm mutants with a specific DCM-associated phenotype. Differential proteomic analysis of cultures grown with DCM and with methanol defined 38 differentially abundant proteins. The 5.5 kb dcm islet directly involved in DCM dehalogenation is the only one of seven gene clusters specific to the DCM response to be localized within the dcm genomic island. The DCM response was shown to involve mainly the core genome of Methylobacterium extorquens, providing new insights on DCM-dependent adjustments of C1 metabolism and gene regulation, and suggesting a specific stress response of Methylobacterium during growth with DCM. Fatty acid, hopanoid and peptidoglycan metabolisms were affected, hinting at the membrane-active effects of DCM due to its solvent properties. A chloride-induced efflux transporter termed CliABC was also newly identified. Thus, DCM dechlorination driven by the dcm islet elicits a complex adaptive response encoded by the core genome common to dechlorinating as well as non-dechlorinating Methylobacterium strains.

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“…1). First, the strain must accommodate the protons and chloride produced intracellularly as a by-product of DCM dehalogenation (22)(23)(24). Additionally, the S-chloromethylglutathione intermediate formed during the dehalogenation reaction is highly reactive and mutagenic (25)(26)(27).…”

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Phylogeny Poorly Predicts the Utility of a Challenging Horizontally Transferred Gene in Methylobacterium Strains

Vuilleumier¹,

Bringel²,

Marx³

2014

Journal of Bacteriology

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cHorizontal gene transfer plays a crucial role in microbial evolution. While much is known about the mechanisms that determine whether physical DNA can be transferred into a new host, the factors determining the utility of the transferred genes are less clear. We have explored this issue using dichloromethane consumption in Methylobacterium strains. Methylobacterium extorquens DM4 expresses a dichloromethane dehalogenase (DcmA) that has been acquired through horizontal gene transfer and allows the strain to grow on dichloromethane as the sole carbon and energy source. We transferred the dcmA gene into six Methylobacterium strains that include both close and distant evolutionary relatives. The transconjugants varied in their ability to grow on dichloromethane, but their fitness on dichloromethane did not correlate with the phylogeny of the parental strains or with any single tested physiological factor. This work highlights an important limiting factor in horizontal gene transfer, namely, the capacity of the recipient strain to accommodate the stress and metabolic disruption resulting from the acquisition of a new enzyme or pathway. Understanding these limitations may help to rationalize historical examples of horizontal transfer and aid deliberate genetic transfers in biotechnology for metabolic engineering.

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Chloride‐associated adaptive response in aerobic methylotrophic dichloromethane‐utilising bacteria

Cited by 18 publications

References 29 publications

Genomic and Transcriptomic Analysis of Growth-Supporting Dehalogenation of Chlorinated Methanes in Methylobacterium

Genomic and Transcriptomic Analysis of Growth-Supporting Dehalogenation of Chlorinated Methanes in Methylobacterium

Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4

Phylogeny Poorly Predicts the Utility of a Challenging Horizontally Transferred Gene in Methylobacterium Strains

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