The origin of aerobic methanotrophy within the Proteobacteria
Abstract
Aerobic methanotrophs play critical roles in the global carbon cycle, but despite their environmental ubiquity, they are phylogenetically restricted. Via bioinformatic analyses, it is shown that methanotrophy likely arose from methylotrophy from the lateral gene transfer of either of the two known forms of methane monooxygenase (particulate and soluble methane monooxygenases). Furthemore, it appears that both known forms of pyrroloquinoline quinone-dependent methanol dehydrogenase (MeDH) found in methanotrophs—the calcium-containing Mxa-MeDH and the rare earth element-containing Xox-MeDH—were likely encoded in the genomes before the acquisition of the methane monooxygenases (MMOs), but that some methanotrophs subsequently received an additional copy of Xox-MeDH-encoding genes via lateral gene transfer. Further, data are presented that indicate the evolution of methanotrophy from methylotrophy not only required lateral transfer of genes encoding for methane monooxygenases, but also likely the pre-existence of a means of collecting copper. Given the emerging interest in valorizing methane via biological platforms, it is recommended that future strategies for heterologous expression of methane monooxygenase for conversion of methane to methanol also include cloning of genes encoding mechanism(s) of copper uptake, especially for expression of particulate methane monooxygenase.
- Authors:
-
- Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, MI, USA 48109-2125
- Department of Biological Sciences, University of Calgary, Calgary, AB, Canada T2N 1N4
- Publication Date:
- Research Org.:
- Univ. of Michigan, Ann Arbor, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1515086
- Alternate Identifier(s):
- OSTI ID: 1691492
- Grant/Contract Number:
- SC0018059; 1724744
- Resource Type:
- Published Article
- Journal Name:
- FEMS Microbiology Letters (Online)
- Additional Journal Information:
- Journal Name: FEMS Microbiology Letters (Online) Journal Volume: 366 Journal Issue: 9; Journal ID: ISSN 1574-6968
- Publisher:
- Federation of European Microbiological Societies
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; methanotrophy; metal uptake; evolution
Citation Formats
Kang, Christina S., Dunfield, Peter F., and Semrau, Jeremy D. The origin of aerobic methanotrophy within the Proteobacteria. Netherlands: N. p., 2019.
Web. doi:10.1093/femsle/fnz096.
Kang, Christina S., Dunfield, Peter F., & Semrau, Jeremy D. The origin of aerobic methanotrophy within the Proteobacteria. Netherlands. https://doi.org/10.1093/femsle/fnz096
Kang, Christina S., Dunfield, Peter F., and Semrau, Jeremy D. Sat .
"The origin of aerobic methanotrophy within the Proteobacteria". Netherlands. https://doi.org/10.1093/femsle/fnz096.
@article{osti_1515086,
title = {The origin of aerobic methanotrophy within the Proteobacteria},
author = {Kang, Christina S. and Dunfield, Peter F. and Semrau, Jeremy D.},
abstractNote = {Aerobic methanotrophs play critical roles in the global carbon cycle, but despite their environmental ubiquity, they are phylogenetically restricted. Via bioinformatic analyses, it is shown that methanotrophy likely arose from methylotrophy from the lateral gene transfer of either of the two known forms of methane monooxygenase (particulate and soluble methane monooxygenases). Furthemore, it appears that both known forms of pyrroloquinoline quinone-dependent methanol dehydrogenase (MeDH) found in methanotrophs—the calcium-containing Mxa-MeDH and the rare earth element-containing Xox-MeDH—were likely encoded in the genomes before the acquisition of the methane monooxygenases (MMOs), but that some methanotrophs subsequently received an additional copy of Xox-MeDH-encoding genes via lateral gene transfer. Further, data are presented that indicate the evolution of methanotrophy from methylotrophy not only required lateral transfer of genes encoding for methane monooxygenases, but also likely the pre-existence of a means of collecting copper. Given the emerging interest in valorizing methane via biological platforms, it is recommended that future strategies for heterologous expression of methane monooxygenase for conversion of methane to methanol also include cloning of genes encoding mechanism(s) of copper uptake, especially for expression of particulate methane monooxygenase.},
doi = {10.1093/femsle/fnz096},
journal = {FEMS Microbiology Letters (Online)},
number = 9,
volume = 366,
place = {Netherlands},
year = {Sat May 04 00:00:00 EDT 2019},
month = {Sat May 04 00:00:00 EDT 2019}
}
https://doi.org/10.1093/femsle/fnz096
Web of Science
Works referenced in this record:
Complexity, connectivity, and duplicability as barriers to lateral gene transfer
journal, January 2007
- Wellner, Alon; Lurie, Mor N.; Gophna, Uri
- Genome Biology, Vol. 8, Issue 8
A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs: Novel monooxygenase in Gamma-MOB
journal, February 2011
- Tavormina, Patricia L.; Orphan, Victoria J.; Kalyuzhnaya, Marina G.
- Environmental Microbiology Reports, Vol. 3, Issue 1
A methanotroph-based biorefinery: Potential scenarios for generating multiple products from a single fermentation
journal, September 2016
- Strong, P. J.; Kalyuzhnaya, M.; Silverman, J.
- Bioresource Technology, Vol. 215
Methanotrophs and copper
journal, July 2010
- Semrau, Jeremy D.; DiSpirito, Alan A.; Yoon, Sukhwan
- FEMS Microbiology Reviews, Vol. 34, Issue 4
An Oxidized Tryptophan Facilitates Copper Binding in Methylococcus capsulatus -secreted Protein MopE
journal, March 2008
- Helland, Ronny; Fjellbirkeland, Anne; Karlsen, Odd Andre
- Journal of Biological Chemistry, Vol. 283, Issue 20
A four-helix bundle stores copper for methane oxidation
journal, August 2015
- Vita, Nicolas; Platsaki, Semeli; Baslé, Arnaud
- Nature, Vol. 525, Issue 7567
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
Aerobic methanol-oxidizing Bacteria âin soil
journal, November 2009
- Kolb, Steffen
- FEMS Microbiology Letters, Vol. 300, Issue 1
Growth yields of methanotrophs: 1. Effect of copper on the energetics of methane oxidation
journal, March 1986
- Leak, David J.; Dalton, Howard
- Applied Microbiology and Biotechnology, Vol. 23, Issue 6
Copper ions as inhibitors of protein C of soluble methane monooxygenase of Methylococcus capsulatus (Bath)
journal, November 1985
- Green, Jeffrey; Prior, Stephen D.; Dalton, Howard
- European Journal of Biochemistry, Vol. 153, Issue 1
Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology
journal, December 2001
- Huelsenbeck, J. P.
- Science, Vol. 294, Issue 5550
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria
journal, September 2004
- Kim, H. J.
- Science, Vol. 305, Issue 5690
The (d)evolution of methanotrophy in the Beijerinckiaceae—a comparative genomics analysis
journal, August 2013
- Tamas, Ivica; Smirnova, Angela V.; He, Zhiguo
- The ISME Journal, Vol. 8, Issue 2
Characterization of a novel facultative Methylocystis species capable of growth on methane, acetate and ethanol: Facultative methanotrophy in a Methylocystis sp.
journal, August 2010
- Im, Jeongdae; Lee, Sung-Woo; Yoon, Sukhwan
- Environmental Microbiology Reports, Vol. 3, Issue 2
Horizontal gene transfer among genomes: The complexity hypothesis
journal, March 1999
- Jain, R.; Rivera, M. C.; Lake, J. A.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 7
Biosynthesis of secondary metabolites in methanotrophs: Biochemical and genetic aspects (Review)
journal, March 2015
- Khmelenina, V. N.; Rozova, O. N.; But, S. Yu.
- Applied Biochemistry and Microbiology, Vol. 51, Issue 2
Marker Exchange Mutagenesis of mxaF , Encoding the Large Subunit of the Mxa Methanol Dehydrogenase, in Methylosinus trichosporium OB3b
journal, December 2015
- Farhan Ul Haque, Muhammad; Gu, Wenyu; DiSpirito, Alan A.
- Applied and Environmental Microbiology, Vol. 82, Issue 5
Cloning and characterization of corA, a gene encoding a copper-repressible polypeptide in the type I methanotroph, Methylomicrobium albus BG8
journal, March 1997
- Berson, Olga; Lidstrom, Mary E.
- FEMS Microbiology Letters, Vol. 148, Issue 2
A redox switch in CopC: An intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites
journal, March 2003
- Arnesano, F.; Banci, L.; Bertini, I.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 7
Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands
journal, July 2006
- Vernikos, Georgios S.; Parkhill, Julian
- Bioinformatics, Vol. 22, Issue 18
Heterologous expression of heterotrophic nitrification genes
journal, December 1997
- Crossman, L. C.; Moir, J. W. B.; Enticknap, J. J.
- Microbiology, Vol. 143, Issue 12
Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases
journal, December 2015
- Larsen, Øivind; Karlsen, Odd A.
- MicrobiologyOpen, Vol. 5, Issue 2
XoxF-Type Methanol Dehydrogenase from the Anaerobic Methanotroph “Candidatus Methylomirabilis oxyfera”
journal, December 2014
- Wu, Ming L.; Wessels, Hans J. C. T.; Pol, Arjan
- Applied and Environmental Microbiology, Vol. 81, Issue 4
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life
journal, September 2013
- Pol, Arjan; Barends, Thomas R. M.; Dietl, Andreas
- Environmental Microbiology, Vol. 16, Issue 1
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference
journal, May 2014
- Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim
- Applied Microbiology and Biotechnology, Vol. 98, Issue 14
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic
journal, March 2009
- Op den Camp, Huub J. M.; Islam, Tajul; Stott, Matthew B.
- Environmental Microbiology Reports, Vol. 1, Issue 5
Bacterial cytosolic proteins with a high capacity for Cu(I) that protect against copper toxicity
journal, December 2016
- Vita, Nicolas; Landolfi, Gianpiero; Baslé, Arnaud
- Scientific Reports, Vol. 6, Issue 1
FeatureExtract--extraction of sequence annotation made easy
journal, July 2005
- Wernersson, R.
- Nucleic Acids Research, Vol. 33, Issue Web Server
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b
journal, January 2016
- Gu, Wenyu; Farhan Ul Haque, Muhammad; Baral, Bipin S.
- Applied and Environmental Microbiology, Vol. 82, Issue 6
Metals and Methanotrophy
journal, January 2018
- Semrau, Jeremy D.; DiSpirito, Alan A.; Gu, Wenyu
- Applied and Environmental Microbiology, Vol. 84, Issue 6
CorA Is a Copper Repressible Surface-Associated Copper(I)-Binding Protein Produced in Methylomicrobium album BG8
journal, February 2014
- Johnson, Kenneth A.; Ve, Thomas; Larsen, Øivind
- PLoS ONE, Vol. 9, Issue 2
Copper and cerium-regulated gene expression in Methylosinus trichosporium OB3b
journal, October 2017
- Gu, Wenyu; Semrau, Jeremy D.
- Applied Microbiology and Biotechnology, Vol. 101, Issue 23-24
A Comparison of Methanobactins from Methylosinus trichosporium OB3b and Methylocystis Strain SB2 Predicts Methanobactins Are Synthesized from Diverse Peptide Precursors Modified To Create a Common Core for Binding and Reducing Copper Ions
journal, November 2010
- Krentz, Benjamin D.; Mulheron, Heidi J.; Semrau, Jeremy D.
- Biochemistry, Vol. 49, Issue 47
Lanthanide-binding peptides and the enzymes that Might Have Been
journal, August 2004
- Lim, S.; Franklin, S. J.
- Cellular and Molecular Life Sciences, Vol. 61, Issue 17
Trichloroethylene degradation and mineralization by pseudomonads and Methylosinus trichosporium OB3b
journal, March 1996
- Sun, A. K.; Wood, T. K.
- Applied Microbiology and Biotechnology, Vol. 45, Issue 1-2
Horizontal gene transfer of three co-inherited methane monooxygenase systems gave rise to methanotrophy in the Proteobacteria
journal, December 2018
- Osborne, Craig D.; Haritos, Victoria S.
- Molecular Phylogenetics and Evolution, Vol. 129
Methane as a Resource: Can the Methanotrophs Add Value?
journal, March 2015
- Strong, P. J.; Xie, S.; Clarke, W. P.
- Environmental Science & Technology, Vol. 49, Issue 7
Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria
journal, May 2012
- El Ghazouani, A.; Basle, A.; Gray, J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 22
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions
journal, December 2016
- Krause, Sascha M. B.; Johnson, Timothy; Samadhi Karunaratne, Yasodara
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 2
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria
journal, March 2010
- Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis
- Nature, Vol. 464, Issue 7288
Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium M ethylomonas denitrificans , sp. nov. type strain FJG1 : Denitrifying metabolism in
journal, March 2015
- Kits, K. Dimitri; Klotz, Martin G.; Stein, Lisa Y.
- Environmental Microbiology, Vol. 17, Issue 9
The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath
journal, September 2003
- Choi, Dong-W.; Kunz, Ryan C.; Boyd, Eric S.
- Journal of Bacteriology, Vol. 185, Issue 19
Carbon source regulation of gene expression in Methylosinus trichosporium OB3b
journal, January 2017
- Farhan Ul Haque, Muhammad; Gu, Wenyu; Baral, Bipin S.
- Applied Microbiology and Biotechnology, Vol. 101, Issue 9
Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures
journal, July 1983
- Stanley, S. H.; Prior, S. D.; Leak, D. J.
- Biotechnology Letters, Vol. 5, Issue 7
Optimization of trichloroethylene degradation using soluble methane monooxygenase ofMethylosinus trichosporium OB3b expressed in recombinant bacteria
journal, August 1996
- Jahng, Deokjin; Kim, Craig S.; Hanson, Richard S.
- Biotechnology and Bioengineering, Vol. 51, Issue 3
Characterization of the role of copCD in copper uptake and the ‘copper-switch’ in Methylosinus trichosporium OB3b
journal, May 2017
- Gu, Wenyu; Farhan Ul Haque, Muhammad; Semrau, Jeremy D.
- FEMS Microbiology Letters, Vol. 364, Issue 10
Lanthanide-Dependent Regulation of Methanol Oxidation Systems in Methylobacterium extorquens AM1 and Their Contribution to Methanol Growth
journal, February 2016
- Vu, Huong N.; Subuyuj, Gabriel A.; Vijayakumar, Srividhya
- Journal of Bacteriology, Vol. 198, Issue 8
MxaY regulates the lanthanide-mediated methanol dehydrogenase switch in Methylomicrobium buryatense
journal, January 2016
- Chu, Frances; Beck, David A. C.; Lidstrom, Mary E.
- PeerJ, Vol. 4
Evolutionary History of Copper Membrane Monooxygenases
journal, October 2018
- Khadka, Roshan; Clothier, Lindsay; Wang, Lin
- Frontiers in Microbiology, Vol. 9
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data
journal, September 2016
- Yu, Guangchuang; Smith, David K.; Zhu, Huachen
- Methods in Ecology and Evolution, Vol. 8, Issue 1
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton
journal, September 2000
- Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap
- Journal of Molecular Biology, Vol. 302, Issue 1
The Methylococcus capsulatus (Bath) Secreted Protein, MopE*, Binds Both Reduced and Oxidized Copper
journal, August 2012
- Ve, Thomas; Mathisen, Karina; Helland, Ronny
- PLoS ONE, Vol. 7, Issue 8