skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transfer of a Catabolic Pathway for Chloromethane in Methylobacterium Strains Highlights Different Limitations for Growth with Chloromethane or with Dichloromethane

Abstract

Chloromethane is an ozone-depleting gas, produced predominantly from natural sources, that provides an important environmental niche for microbes capable of consuming it. Chloromethane catabolism has been difficult to study owing to the challenging genetics of its native microbial hosts. Since the pathways for chloromethane catabolism show evidence of horizontal gene transfer, we reproduced this transfer process in the laboratory to generate new chloromethane-catabolizing strains in tractable hosts. Here, we demonstrate that six putative accessory genes improve chloromethane catabolism, though heterologous expression of only one of the six is strictly necessary for growth on chloromethane. In contrast to growth of Methylobacterium strains with the closely-related compound dichloromethane, we find that chloride export does not limit growth on chloromethane and, in general, that the ability of a strain to grow on dichloromethane is uncorrelated with its ability to grow on chloromethane. Finally, this heterologous expression system allows us to investigate the components required for effective chloromethane catabolism and the factors that limit effective catabolism after horizontal transfer.

Authors:
 [1];  [2];  [2];  [3]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Harvard Univ., Cambridge, MA (United States)
  2. Univ. of Strasbourg (France)
  3. Harvard Univ., Cambridge, MA (United States); Univ. of Idaho, Moscow, ID (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1265893
Grant/Contract Number:  
AC05-00OR22725; F32 GM106629
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Michener, Joshua K., Vuilleumier, Stéphane, Bringel, Françoise, and Marx, Christopher J. Transfer of a Catabolic Pathway for Chloromethane in Methylobacterium Strains Highlights Different Limitations for Growth with Chloromethane or with Dichloromethane. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.01116.
Michener, Joshua K., Vuilleumier, Stéphane, Bringel, Françoise, & Marx, Christopher J. Transfer of a Catabolic Pathway for Chloromethane in Methylobacterium Strains Highlights Different Limitations for Growth with Chloromethane or with Dichloromethane. United States. https://doi.org/10.3389/fmicb.2016.01116
Michener, Joshua K., Vuilleumier, Stéphane, Bringel, Françoise, and Marx, Christopher J. 2016. "Transfer of a Catabolic Pathway for Chloromethane in Methylobacterium Strains Highlights Different Limitations for Growth with Chloromethane or with Dichloromethane". United States. https://doi.org/10.3389/fmicb.2016.01116. https://www.osti.gov/servlets/purl/1265893.
@article{osti_1265893,
title = {Transfer of a Catabolic Pathway for Chloromethane in Methylobacterium Strains Highlights Different Limitations for Growth with Chloromethane or with Dichloromethane},
author = {Michener, Joshua K. and Vuilleumier, Stéphane and Bringel, Françoise and Marx, Christopher J.},
abstractNote = {Chloromethane is an ozone-depleting gas, produced predominantly from natural sources, that provides an important environmental niche for microbes capable of consuming it. Chloromethane catabolism has been difficult to study owing to the challenging genetics of its native microbial hosts. Since the pathways for chloromethane catabolism show evidence of horizontal gene transfer, we reproduced this transfer process in the laboratory to generate new chloromethane-catabolizing strains in tractable hosts. Here, we demonstrate that six putative accessory genes improve chloromethane catabolism, though heterologous expression of only one of the six is strictly necessary for growth on chloromethane. In contrast to growth of Methylobacterium strains with the closely-related compound dichloromethane, we find that chloride export does not limit growth on chloromethane and, in general, that the ability of a strain to grow on dichloromethane is uncorrelated with its ability to grow on chloromethane. Finally, this heterologous expression system allows us to investigate the components required for effective chloromethane catabolism and the factors that limit effective catabolism after horizontal transfer.},
doi = {10.3389/fmicb.2016.01116},
url = {https://www.osti.gov/biblio/1265893}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 7,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

New insight into the atmospheric chloromethane budget gained using stable carbon isotope ratios
journal, January 2005


Phylogeny Poorly Predicts the Utility of a Challenging Horizontally Transferred Gene in Methylobacterium Strains
journal, March 2014


Development of an Optimized Medium, Strain and High-Throughput Culturing Methods for Methylobacterium extorquens
journal, April 2013


Complete Genome Sequence of the Chloromethane-Degrading Hyphomicrobium sp. Strain MC1
journal, August 2011


Probing the diversity of chloromethane-degrading bacteria by comparative genomics and isotopic fractionation
journal, October 2014


Development of an Optimized Medium, Strain and High-Throughput Culturing Methods for Methylobacterium extorquens
journal, April 2013


Complete Genome Sequences of Six Strains of the Genus Methylobacterium
journal, August 2012


Methyl Chloride: Naturally Occurring Toxicant and C-1 Growth Substrate
journal, April 1986


Microbial growth on C1 compounds. 1. Isolation and characterization of Pseudomonas AM 1
journal, December 1961


Analysis of genes involved in methyl halide degradation in Aminobacter lissarensis CC495
journal, October 2005


Chloromethane Metabolism by Methylobacterium sp. Strain CM4
journal, May 1998


Molecular cloning of a malyl coenzyme A lyase gene from Pseudomonas sp. strain AM1, a facultative methylotroph.
journal, January 1984


Isolation and initial characterization of aerobic chloromethane-utilizing bacteria
journal, September 1996


New insight into the atmospheric chloromethane budget gained using stable carbon isotope ratios
journal, January 2005


Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides×nigra DN34)
journal, July 2004


A corrinoid-dependent catabolic pathway for growth of a Methylobacterium strain with chloromethane
journal, April 1999


A corrinoid-dependent catabolic pathway for growth of a Methylobacterium strain with chloromethane
journal, April 1999


Specialized bacterial strains for the removal of dichloromethane from industrial waste
journal, January 1985


Formate as the Main Branch Point for Methylotrophic Metabolism in Methylobacterium extorquens AM1
journal, May 2008


Specialized bacterial strains for the removal of dichloromethane from industrial waste
journal, January 1985


Chloromethane-Induced Genes Define a Third C1 Utilization Pathway in Methylobacterium chloromethanicum CM4
journal, July 2002


A strong source of methyl chloride to the atmosphere from tropical coastal land
journal, January 2000


ASYMMETRIC, BIMODAL TRADE-OFFS DURING ADAPTATION OF METHYLOBACTERIUM TO DISTINCT GROWTH SUBSTRATES
journal, November 2009


Flux Analysis Uncovers Key Role of Functional Redundancy in Formaldehyde Metabolism
journal, January 2005


Methyl Chloride: Naturally Occurring Toxicant and C-1 Growth Substrate
journal, April 1986


Analysis of genes involved in methyl halide degradation in Aminobacter lissarensis CC495
journal, October 2005


Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides×nigra DN34)
journal, July 2004


Isolation and initial characterization of aerobic chloromethane-utilizing bacteria
journal, September 1996


A strong source of methyl chloride to the atmosphere from tropical coastal land
journal, January 2000


Flux Analysis Uncovers Key Role of Functional Redundancy in Formaldehyde Metabolism
journal, January 2005


Chloromethane:tetrahydrofolate methyl transfer by two proteins from Methylobacterium chloromethanicum strain CM4: Chloromethane dehalogenase
journal, May 2001


Microbial growth on C1 compounds. 1. Isolation and characterization of Pseudomonas AM 1
journal, December 1961


ASYMMETRIC, BIMODAL TRADE-OFFS DURING ADAPTATION OF METHYLOBACTERIUM TO DISTINCT GROWTH SUBSTRATES
journal, November 2009


Probing the diversity of chloromethane-degrading bacteria by comparative genomics and isotopic fractionation
journal, October 2014


Molecular cloning of a malyl coenzyme A lyase gene from Pseudomonas sp. strain AM1, a facultative methylotroph.
journal, January 1984