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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 Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1265893
Grant/Contract Number:  
AC05-00OR22725; F32 GM106629
Resource Type:
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. https://doi.org/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.. Tue . "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},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {7}
}

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Works referenced in this record:

Mapping the Fitness Landscape of Gene Expression Uncovers the Cause of Antagonism and Sign Epistasis between Adaptive Mutations
journal, February 2014


Synthetic and Evolutionary Construction of a Chlorate-Reducing Shewanella oneidensis MR-1
journal, May 2015

  • Clark, Iain C.; Melnyk, Ryan A.; Youngblut, Matthew D.
  • mBio, Vol. 6, Issue 3
  • DOI: 10.1128/mBio.00282-15

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

  • Crowther, G. J.; Kosaly, G.; Lidstrom, M. E.
  • Journal of Bacteriology, Vol. 190, Issue 14, p. 5057-5062
  • DOI: 10.1128/JB.00228-08

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


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


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


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


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

  • Keppler, F.; Harper, D. B.; Röckmann, T.
  • Atmospheric Chemistry and Physics, Vol. 5, Issue 9
  • DOI: 10.5194/acp-5-2403-2005

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


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

  • Marx, C. J.; Bringel, F.; Chistoserdova, L.
  • Journal of Bacteriology, Vol. 194, Issue 17
  • DOI: 10.1128/JB.01009-12

Purification of the Formate-Tetrahydrofolate Ligasefrom Methylobacterium extorquens AM1 and Demonstrationof Its Requirement for MethylotrophicGrowth
journal, December 2003


Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria
journal, August 2001


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


Chloromethane Utilization Gene Cluster fromHyphomicrobium chloromethanicum Strain CM2T and Development of Functional Gene Probes To Detect Halomethane-Degrading Bacteria
journal, January 2001

  • McAnulla, Craig; Woodall, Claire A.; McDonald, Ian R.
  • Applied and Environmental Microbiology, Vol. 67, Issue 1
  • DOI: 10.1128/AEM.67.1.307-316.2001

Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post–transfer refinement
journal, November 2014

  • Michener, Joshua K.; Camargo Neves, Aline A.; Vuilleumier, Stéphane
  • eLife, Vol. 3
  • DOI: 10.7554/eLife.04279

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

  • Michener, J. K.; Vuilleumier, S.; Bringel, F.
  • Journal of Bacteriology, Vol. 196, Issue 11
  • DOI: 10.1128/JB.00034-14

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

  • Nadalig, Thierry; Greule, Markus; Bringel, Françoise
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00523

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


Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halide-oxidizing bacteria: Novel marine methyl halide-oxidizing bacteria
journal, March 2005


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


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


Methylotrophic MethylobacteriumBacteria Nodulate and Fix Nitrogen in Symbiosis with Legumes
journal, January 2001


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

  • Van Aken, Benoit; Peres, Caroline M.; Doty, Sharon Lafferty
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 54, Issue 4
  • DOI: 10.1099/ijs.0.02796-0

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

  • Vannelli, T.; Messmer, M.; Studer, A.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 8
  • DOI: 10.1073/pnas.96.8.4615

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

  • Vuilleumier, S.; Nadalig, T.; Farhan Ul Haque, M.
  • Journal of Bacteriology, Vol. 193, Issue 18
  • DOI: 10.1128/JB.05627-11

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


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

  • Yokouchi, Y.; Noijiri, Y.; Barrie, L. A.
  • Nature, Vol. 403, Issue 6767
  • DOI: 10.1038/35002049

    Works referencing / citing this record:

    Methanol consumption drives the bacterial chloromethane sink in a forest soil
    journal, July 2018


    Rapid, Parallel Identification of Catabolism Pathways of Lignin-Derived Aromatic Compounds in Novosphingobium aromaticivorans
    journal, September 2018

    • Cecil, Jacob H.; Garcia, David C.; Giannone, Richard J.
    • Applied and Environmental Microbiology, Vol. 84, Issue 22
    • DOI: 10.1128/aem.01185-18