Evidence for methanobactin “Theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation

Kang-Yun, Christina S.; Liang, Xujun; Dershwitz, Philip; Gu, Wenyu; Schepers, Aloys; Flatley, Andrew; Lichtmannegger, Josef; Zischka, Hans; Zhang, Lijie; Lu, Xia; Gu, Baohua; Ledesma, Joshua C.; Pelger, Daly J.; DiSpirito, Alan A.; Semrau, Jeremy D.

doi:10.1038/s41396-021-01062-1

Title: Evidence for methanobactin “Theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation

Journal Article · Wed Jul 21 00:00:00 EDT 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-01062-1· OSTI ID:2280747

; Liang, Xujun;

;

; Schepers, Aloys;

; Lichtmannegger, Josef;

;

; Ledesma, Joshua C.; Pelger, Daly J.; DiSpirito, Alan A.;

Abstract Aerobic methanotrophy is strongly controlled by copper, and methanotrophs are known to use different mechanisms for copper uptake. Some methanotrophs secrete a modified polypeptide—methanobactin—while others utilize a surface-bound protein (MopE) and a secreted form of it (MopE*) for copper collection. As different methanotrophs have different means of sequestering copper, competition for copper significantly impacts methanotrophic activity. Herein, we show that Methylomicrobium album BG8, Methylocystis sp. strain Rockwell, and Methylococcus capsulatus Bath, all lacking genes for methanobactin biosynthesis, are not limited for copper by multiple forms of methanobactin. Interestingly, Mm. album BG8 and Methylocystis sp. strain Rockwell were found to have genes similar to mbnT that encodes for a TonB-dependent transporter required for methanobactin uptake. Data indicate that these methanotrophs “steal” methanobactin and such “theft” enhances the ability of these strains to degrade methylmercury, a potent neurotoxin. Further, when mbnT was deleted in Mm. album BG8, methylmercury degradation in the presence of methanobactin was indistinguishable from when MB was not added. Mc. capsulatus Bath lacks anything similar to mbnT and was unable to degrade methylmercury either in the presence or absence of methanobactin. Rather, Mc. capsulatus Bath appears to rely on MopE/MopE* for copper collection. Finally, not only does Mm. album BG8 steal methanobactin, it synthesizes a novel chalkophore, suggesting that some methanotrophs utilize both competition and cheating strategies for copper collection. Through a better understanding of these strategies, methanotrophic communities may be more effectively manipulated to reduce methane emissions and also enhance mercury detoxification in situ.

View Journal Article

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF)

Grant/Contract Number:: SC00018059; AC05-00OR22725; 1724430; 1724744; SC0018059; SC0020174

OSTI ID:: 2280747

Alternate ID(s):: OSTI ID: 1814404

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Vol. 16 Journal Issue: 1; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (58)

Factors affecting competition between type I and type II methanotrophs in two-organism, continuous-flow reactors Graham, DavidW.; Chaudhary, JayeshA.; Hanson, RichardS. Microbial Ecology, Vol. 25, Issue 1 https://doi.org/10.1007/BF00182126	journal	January 1993
Methanotrophs and copper Semrau, Jeremy D.; DiSpirito, Alan A.; Yoon, Sukhwan FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2010.00212.x	journal	July 2010
An Oxidized Tryptophan Facilitates Copper Binding in Methylococcus capsulatus -secreted Protein MopE Helland, Ronny; Fjellbirkeland, Anne; Karlsen, Odd Andre Journal of Biological Chemistry, Vol. 283, Issue 20 https://doi.org/10.1074/jbc.M800340200	journal	March 2008
Mixed Pollutant Degradation by Methylosinus trichosporium OB3b Expressing either Soluble or Particulate Methane Monooxygenase: Can the Tortoise Beat the Hare? Lee, S. -W.; Keeney, D. R.; Lim, D. -H. Applied and Environmental Microbiology, Vol. 72, Issue 12 https://doi.org/10.1128/AEM.01604-06	journal	September 2006
Siderophores in environmental research: roles and applications: Siderophores in environmental research Ahmed, E.; Holmström, S. J. M. Microbial Biotechnology, Vol. 7, Issue 3 https://doi.org/10.1111/1751-7915.12117	journal	February 2014
Social evolution theory for microorganisms West, Stuart A.; Griffin, Ashleigh S.; Gardner, Andy Nature Reviews Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/nrmicro1461	journal	August 2006
Quantum Refinement Does Not Support Dinuclear Copper Sites in Crystal Structures of Particulate Methane Monooxygenase Cao, Lili; Caldararu, Octav; Rosenzweig, Amy C. Angewandte Chemie International Edition, Vol. 57, Issue 1 https://doi.org/10.1002/anie.201708977	journal	December 2017
Enrichment, Isolation and Some Properties of Methane-utilizing Bacteria Whittenbury, R.; Phillips, K. C.; Wilkinson, J. F. Journal of General Microbiology, Vol. 61, Issue 2 https://doi.org/10.1099/00221287-61-2-205	journal	May 1970
Oxygen Generation via Water Splitting by a Novel Biogenic Metal Ion-Binding Compound Dershwitz, Philip; Bandow, Nathan L.; Yang, Junwon Applied and Environmental Microbiology, Vol. 87, Issue 14 https://doi.org/10.1128/AEM.00286-21	journal	June 2021
Effect of Exogenous Siderophores on Iron Uptake Activity of Marine Bacteria under Iron-Limited Conditions Guan, L. L.; Kanoh, K.; Kamino, K. Applied and Environmental Microbiology, Vol. 67, Issue 4 https://doi.org/10.1128/AEM.67.4.1710-1717.2001	journal	April 2001
Biochemistry of the Soluble Methane Monooxygenase Lipscomb, J. D. Annual Review of Microbiology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.mi.48.100194.002103	journal	October 1994
Analyzing real-time PCR data by the comparative CT method Schmittgen, Thomas D.; Livak, Kenneth J. Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.73	journal	June 2008
Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs: Copper-switch in methanotrophy Semrau, Jeremy D.; Jagadevan, Sheeja; DiSpirito, Alan A. Environmental Microbiology https://doi.org/10.1111/1462-2920.12150	journal	May 2013
Mössbauer Studies of the Membrane-Associated Methane Monooxygenase from Methylococcus capsulatus Bath: Evidence for a Diiron Center Martinho, Marlène; Choi, Dong W.; DiSpirito, Alan A. Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja077682b	journal	December 2007
Growth yields of methanotrophs: 1. Effect of copper on the energetics of methane oxidation Leak, David J.; Dalton, Howard Applied Microbiology and Biotechnology, Vol. 23, Issue 6 https://doi.org/10.1007/BF02346062	journal	March 1986
Methanobactin from Methylocystis sp. Strain SB2 Affects Gene Expression and Methane Monooxygenase Activity in Methylosinus trichosporium OB3b Farhan Ul-Haque, Muhammad; Kalidass, Bhagyalakshmi; Vorobev, Alexey Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/AEM.03981-14	journal	January 2015
Methanobactin and the Link between Copper and Bacterial Methane Oxidation DiSpirito, Alan A.; Semrau, Jeremy D.; Murrell, J. Colin Microbiology and Molecular Biology Reviews, Vol. 80, Issue 2 https://doi.org/10.1128/MMBR.00058-15	journal	March 2016
Methanobactin transport machinery Dassama, Laura M. K.; Kenney, Grace E.; Ro, Soo Y. Proceedings of the National Academy of Sciences, Vol. 113, Issue 46 https://doi.org/10.1073/pnas.1603578113	journal	November 2016
Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury Yin, Xixiang; Wang, Lihong; Zhang, Lijie Applied and Environmental Microbiology, Vol. 86, Issue 11 https://doi.org/10.1128/AEM.00122-20	journal	May 2020
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria Kim, H. J. Science, Vol. 305, Issue 5690 https://doi.org/10.1126/science.1098322	journal	September 2004
Bacterial iron homeostasis Andrews, Simon C.; Robinson, Andrea K.; Rodríguez-Quiñones, Francisco FEMS Microbiology Reviews, Vol. 27, Issue 2-3 https://doi.org/10.1016/S0168-6445(03)00055-X	journal	June 2003
Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves Sprouffske, Kathleen; Wagner, Andreas BMC Bioinformatics, Vol. 17, Issue 1 https://doi.org/10.1186/s12859-016-1016-7	journal	April 2016
Isolation of Methanobactin from the Spent Media of Methane-Oxidizing Bacteria Bandow, Nathan L.; Gallagher, Warren H.; Behling, Lee Methods in Methane Metabolism, Part B: Methanotrophy https://doi.org/10.1016/B978-0-12-386905-0.00017-6	book	January 2011
Interspecies Chemical Signaling in a Methane-Oxidizing Bacterial Community Puri, Aaron W.; Liu, Darren; Schaefer, Amy L. Applied and Environmental Microbiology, Vol. 85, Issue 7 https://doi.org/10.1128/AEM.02702-18	journal	February 2019
Competition between Metals for Binding to Methanobactin Enables Expression of Soluble Methane Monooxygenase in the Presence of Copper Kalidass, Bhagyalakshmi; Ul-Haque, Muhammad Farhan; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 81, Issue 3 https://doi.org/10.1128/AEM.03151-14	journal	November 2014
Cloning and characterization of corA, a gene encoding a copper-repressible polypeptide in the type I methanotroph, Methylomicrobium albus BG8 Berson, Olga; Lidstrom, Mary E. FEMS Microbiology Letters, Vol. 148, Issue 2 https://doi.org/10.1111/j.1574-6968.1997.tb10284.x	journal	March 1997
Acquisition of iron by the non-siderophore-producing Pseudomonas fragi Champomier-Verges, M. -C.; Stintzi, A.; Meyer, J. -M. Microbiology, Vol. 142, Issue 5 https://doi.org/10.1099/13500872-142-5-1191	journal	May 1996
Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2 Bandow, Nathan; Gilles, Valerie S.; Freesmeier, Brittani Journal of Inorganic Biochemistry, Vol. 110 https://doi.org/10.1016/j.jinorgbio.2012.02.002	journal	May 2012
The Surface-Associated and Secreted MopE Protein of Methylococcus capsulatus (Bath) Responds to Changes in the Concentration of Copper in the Growth Medium Karlsen, O. A.; Berven, F. S.; Stafford, G. P. Applied and Environmental Microbiology, Vol. 69, Issue 4 https://doi.org/10.1128/AEM.69.4.2386-2388.2003	journal	April 2003
Widespread soil bacterium that oxidizes atmospheric methane Tveit, Alexander T.; Hestnes, Anne Grethe; Robinson, Serina L. Proceedings of the National Academy of Sciences, Vol. 116, Issue 17 https://doi.org/10.1073/pnas.1817812116	journal	April 2019
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b Gu, Wenyu; Farhan Ul Haque, Muhammad; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 82, Issue 6 https://doi.org/10.1128/AEM.03884-15	journal	January 2016
Metals and Methanotrophy Semrau, Jeremy D.; DiSpirito, Alan A.; Gu, Wenyu Applied and Environmental Microbiology, Vol. 84, Issue 6 https://doi.org/10.1128/AEM.02289-17	journal	January 2018
Methylmercury uptake and degradation by methanotrophs Lu, Xia; Gu, Wenyu; Zhao, Linduo Science Advances, Vol. 3, Issue 5 https://doi.org/10.1126/sciadv.1700041	journal	May 2017
Feasibility of atmospheric methane removal using methanotrophic biotrickling filters Yoon, Sukhwan; Carey, Jeffrey N.; Semrau, Jeremy D. Applied Microbiology and Biotechnology, Vol. 83, Issue 5 https://doi.org/10.1007/s00253-009-1977-9	journal	April 2009
An Aminotransferase is Responsible for the Deamination of the N-terminal Leucine and Required for Formation of Oxazolone Ring A in Methanobactin of Methylosinus trichosporium OB3b Gu, Wenyu; Baral, Bipin S.; DiSpirito, Alan A. Applied and Environmental Microbiology https://doi.org/10.1128/AEM.02619-16	journal	October 2016
Derivatization of Polyvinylidene Difluoride Membranes for the Solid-Phase Sequence Analysis of a Phosphorylated Sea Urchin Embryo Histone H1 Peptide Rodrigues, J. D.; Combrink, J.; Brandt, W. F. Analytical Biochemistry, Vol. 216, Issue 2 https://doi.org/10.1006/abio.1994.1054	journal	February 1994
Thiol-Facilitated Cell Export and Desorption of Methylmercury by Anaerobic Bacteria Lin, Hui; Lu, Xia; Liang, Liyuan Environmental Science & Technology Letters, Vol. 2, Issue 10 https://doi.org/10.1021/acs.estlett.5b00209	journal	September 2015
Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations Cordero, O. X.; Ventouras, L. -A.; DeLong, E. F. Proceedings of the National Academy of Sciences, Vol. 109, Issue 49 https://doi.org/10.1073/pnas.1213344109	journal	November 2012
Anaerobic Mercury Methylation and Demethylation by Geobacter bemidjiensis Bem Lu, Xia; Liu, Yurong; Johs, Alexander Environmental Science & Technology, Vol. 50, Issue 8 https://doi.org/10.1021/acs.est.6b00401	journal	April 2016
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities Butaitė, Elena; Baumgartner, Michael; Wyder, Stefan Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00509-4	journal	September 2017
The origin of aerobic methanotrophy within the Proteobacteria Kang, Christina S.; Dunfield, Peter F.; Semrau, Jeremy D. FEMS Microbiology Letters, Vol. 366, Issue 9 https://doi.org/10.1093/femsle/fnz096	journal	May 2019
Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b Gu, Wenyu; Farhan Ul Haque, Muhammad; DiSpirito, Alan A. FEMS Microbiology Letters, Vol. 363, Issue 13 https://doi.org/10.1093/femsle/fnw129	journal	May 2016
Effect of Copper on Methylomonas albus BG8 † Collins, Mary Lynne Perille; Buchholz, Lorie A.; Remsen, Charles C. Applied and Environmental Microbiology, Vol. 57, Issue 4 https://doi.org/10.1128/aem.57.4.1261-1264.1991	journal	January 1991
Unravelling the Identity, Metabolic Potential and Global Biogeography of the Atmospheric Methane-Oxidizing Upland Soil Cluster α: Illuminating the USCα methanotrophs from soil Pratscher, Jennifer; Vollmers, John; Wiegand, Sandra Environmental Microbiology, Vol. 20, Issue 3 https://doi.org/10.1111/1462-2920.14036	journal	January 2018
The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath Choi, Dong-W.; Kunz, Ryan C.; Boyd, Eric S. Journal of Bacteriology, Vol. 185, Issue 19 https://doi.org/10.1128/JB.185.19.5755-5764.2003	journal	September 2003
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Spectral and thermodynamic properties of methanobactin from γ-proteobacterial methane oxidizing bacteria: A case for copper competition on a molecular level Choi, Dong W.; Bandow, Nathan L.; McEllistrem, Marcus T. Journal of Inorganic Biochemistry, Vol. 104, Issue 12 https://doi.org/10.1016/j.jinorgbio.2010.08.002	journal	December 2010
Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils Cai, Yuanfeng; Zheng, Yan; Bodelier, Paul L. E. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11728	journal	June 2016
Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures Stanley, S. H.; Prior, S. D.; Leak, D. J. Biotechnology Letters, Vol. 5, Issue 7 https://doi.org/10.1007/BF00132233	journal	July 1983
Methanobactin from methanotrophs: genetics, structure, function and potential applications Semrau, Jeremy D.; DiSpirito, Alan A.; Obulisamy, Parthiba Karthikeyan FEMS Microbiology Letters, Vol. 367, Issue 5 https://doi.org/10.1093/femsle/fnaa045	journal	March 2020
Cooperation and competition in pathogenic bacteria Griffin, Ashleigh S.; West, Stuart A.; Buckling, Angus Nature, Vol. 430, Issue 7003 https://doi.org/10.1038/nature02744	journal	August 2004
Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2 Baani, M.; Liesack, W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0702643105	journal	July 2008
The biosynthesis of methanobactin Kenney, Grace E.; Dassama, Laura M. K.; Pandelia, Maria-Eirini Science, Vol. 359, Issue 6382 https://doi.org/10.1126/science.aap9437	journal	March 2018
The Social Lives of Microbes West, Stuart A.; Diggle, Stephen P.; Buckling, Angus Annual Review of Ecology, Evolution, and Systematics, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.ecolsys.38.091206.095740	journal	December 2007
Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands Chowdhury, Taniya Roy; Dick, Richard P. Applied Soil Ecology, Vol. 65 https://doi.org/10.1016/j.apsoil.2012.12.014	journal	March 2013
The Methylococcus capsulatus (Bath) Secreted Protein, MopE*, Binds Both Reduced and Oxidized Copper Ve, Thomas; Mathisen, Karina; Helland, Ronny PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0043146	journal	August 2012
The C-terminal part of the surface-associated protein MopE of the methanotroph Methylococcus capsulatus (Bath) is secreted into the growth medium Fjellbirkeland, Anne; Kruger, Per; Bemanian, Vahid Archives of Microbiology, Vol. 176, Issue 3 https://doi.org/10.1007/s002030100307	journal	September 2001
Methanobactin reverses acute liver failure in a rat model of Wilson disease Lichtmannegger, Josef; Leitzinger, Christin; Wimmer, Ralf Journal of Clinical Investigation, Vol. 126, Issue 7 https://doi.org/10.1172/JCI85226	journal	June 2016

Similar Records

Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury

Journal Article · Tue May 19 00:00:00 EDT 2020 · Applied and Environmental Microbiology · OSTI ID:2280747

Yin, Xixiang; Wang, Lihong; Zhang, Lijie; +6 more

Combined Effects of Carbon and Nitrogen Source to Optimize Growth of Proteobacterial Methanotrophs

Journal Article · Tue Sep 25 00:00:00 EDT 2018 · Frontiers in Microbiology · OSTI ID:2280747

Tays, Catherine; Guarnieri, Michael T.; Sauvageau, Dominic; +1 more

Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’

Journal Article · Wed Oct 20 00:00:00 EDT 2021 · Applied and Environmental Microbiology · OSTI ID:2280747

Peng, Peng; Kang-Yun, Christina S.; Chang, Jin; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bacterial genetics
biogeochemistry
soil microbiology

Title: Evidence for methanobactin “Theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation

Citation Formats

References (58)

Similar Records

Related Subjects