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

Title: Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20Z R

Abstract

Background: Rare Earth Elements (REEs) control methanol utilization in both methane- and methanol-utilizing microbes. It has been established that the addition of REEs leads to the transcriptional repression of MxaFI-MeDH (a two-subunit methanol dehydrogenase, calcium-dependent) and the activation of XoxF-MeDH (a one-subunit methanol dehydrogenase, lanthanumdependent). Both enzymes are pyrroquinoline quinone-dependent alcohol dehydrogenases and show significant homology; however, they display different kinetic properties and substrate specificities. This study investigates the impact of the MxaFI to XoxF switch on the behavior of metabolic networks at a global scale. Results: In this study we investigated the steady-state growth of Methylomicrobium alcaliphilum 20Z R in media containing calcium (Ca) or lanthanum (La, a REE element). We found that cells supplemented with La show a higher growth rate compared to Ca-cultures; however, the efficiency of carbon conversion, estimated as biomass yield, is higher in cells grown with Ca. Three complementary global-omics approaches—RNA-seq transcriptomics, proteomics, and metabolomics—were applied to investigate the mechanisms of improved growth vs carbon conversion. Cells grown with La showed the transcriptional activation of the xoxF gene, a homologue of the formaldehyde-activating enzyme (fae2), a putative transporter, genes for hemin-transport proteins, and nitrate reductase. In contrast, genes for mxaFI and associated cytochrome (mxaG)more » expression were downregulated. Proteomic profiling suggested additional adjustments of the metabolic network at the protein level, including carbon assimilation pathways, electron transport systems, and the tricarboxylic acid (TCA) cycle. Discord between gene expression and protein abundance changes points toward the possibility of post-transcriptional control of the related systems including key enzymes of the TCA cycle and a set of electron-transport carriers. Metabolomic data followed proteomics and showed the reduction of the ribulosemonophosphate (RuMP) pathway intermediates and the increase of the TCA cycle metabolites. Conclusions: Cells exposed to REEs display higher rates of growth but have lower carbon conversion efficiency compared to cells supplemented with Ca. The most plausible explanation for these physiological changes is an increased conversion of methanol into formate by XoxF-MeDH, which further stimulates methane oxidation but limits both the supply of reducing power and flux of formaldehyde into the RuMP pathway.« less

Authors:
 [1];  [2];  [2];  [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [4];  [2]
  1. San Diego State Univ., San Diego, CA (United States); Institute of Cytology and Genetics SB RAS, Novosibirsk (Russia); Novosibirsk State University (Russia)
  2. San Diego State Univ., San Diego, CA (United States)
  3. Institute of Cytology and Genetics SB RAS, Novosibirsk (Russia)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1507987
Report Number(s):
PNNL-SA-139645
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Akberdin, Ilya R., Collins, David A., Hamilton, Richard, Oshchepkov, Dmitry Y., Shukla, Anil K., Nicora, Carrie D., Nakayasu, Ernesto S., Adkins, Joshua N., and Kalyuzhnaya, Marina G. Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.02735.
Akberdin, Ilya R., Collins, David A., Hamilton, Richard, Oshchepkov, Dmitry Y., Shukla, Anil K., Nicora, Carrie D., Nakayasu, Ernesto S., Adkins, Joshua N., & Kalyuzhnaya, Marina G. Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR. United States. doi:10.3389/fmicb.2018.02735.
Akberdin, Ilya R., Collins, David A., Hamilton, Richard, Oshchepkov, Dmitry Y., Shukla, Anil K., Nicora, Carrie D., Nakayasu, Ernesto S., Adkins, Joshua N., and Kalyuzhnaya, Marina G. Tue . "Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR". United States. doi:10.3389/fmicb.2018.02735. https://www.osti.gov/servlets/purl/1507987.
@article{osti_1507987,
title = {Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR},
author = {Akberdin, Ilya R. and Collins, David A. and Hamilton, Richard and Oshchepkov, Dmitry Y. and Shukla, Anil K. and Nicora, Carrie D. and Nakayasu, Ernesto S. and Adkins, Joshua N. and Kalyuzhnaya, Marina G.},
abstractNote = {Background: Rare Earth Elements (REEs) control methanol utilization in both methane- and methanol-utilizing microbes. It has been established that the addition of REEs leads to the transcriptional repression of MxaFI-MeDH (a two-subunit methanol dehydrogenase, calcium-dependent) and the activation of XoxF-MeDH (a one-subunit methanol dehydrogenase, lanthanumdependent). Both enzymes are pyrroquinoline quinone-dependent alcohol dehydrogenases and show significant homology; however, they display different kinetic properties and substrate specificities. This study investigates the impact of the MxaFI to XoxF switch on the behavior of metabolic networks at a global scale. Results: In this study we investigated the steady-state growth of Methylomicrobium alcaliphilum 20ZR in media containing calcium (Ca) or lanthanum (La, a REE element). We found that cells supplemented with La show a higher growth rate compared to Ca-cultures; however, the efficiency of carbon conversion, estimated as biomass yield, is higher in cells grown with Ca. Three complementary global-omics approaches—RNA-seq transcriptomics, proteomics, and metabolomics—were applied to investigate the mechanisms of improved growth vs carbon conversion. Cells grown with La showed the transcriptional activation of the xoxF gene, a homologue of the formaldehyde-activating enzyme (fae2), a putative transporter, genes for hemin-transport proteins, and nitrate reductase. In contrast, genes for mxaFI and associated cytochrome (mxaG) expression were downregulated. Proteomic profiling suggested additional adjustments of the metabolic network at the protein level, including carbon assimilation pathways, electron transport systems, and the tricarboxylic acid (TCA) cycle. Discord between gene expression and protein abundance changes points toward the possibility of post-transcriptional control of the related systems including key enzymes of the TCA cycle and a set of electron-transport carriers. Metabolomic data followed proteomics and showed the reduction of the ribulosemonophosphate (RuMP) pathway intermediates and the increase of the TCA cycle metabolites. Conclusions: Cells exposed to REEs display higher rates of growth but have lower carbon conversion efficiency compared to cells supplemented with Ca. The most plausible explanation for these physiological changes is an increased conversion of methanol into formate by XoxF-MeDH, which further stimulates methane oxidation but limits both the supply of reducing power and flux of formaldehyde into the RuMP pathway.},
doi = {10.3389/fmicb.2018.02735},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {11}
}

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

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Figures / Tables:

Table 1 Table 1: Growth parameters and substrate consumption in continuous bioreactor cultures of M. alcaliphilum 20ZR supplemented with Ca or La.

Save / Share:

Works referenced in this record:

XoxF Acts as the Predominant Methanol Dehydrogenase in the Type I Methanotroph Methylomicrobium buryatense
journal, February 2016

  • Chu, Frances; Lidstrom, Mary E.
  • Journal of Bacteriology, Vol. 198, Issue 8
  • DOI: 10.1128/JB.00959-15

A methanotroph-based biorefinery: Potential scenarios for generating multiple products from a single fermentation
journal, September 2016


Primary characterization of dominant cell surface proteins of halotolerant methanotroph Methylomicrobium alcaliphilum 20Z
journal, October 2011


Identification of a bacterial di-haem cytochrome c peroxidase from Methylomicrobium album BG8
journal, June 2010


The structure and mechanism of methanol dehydrogenase
journal, April 2003

  • Anthony, Christopher; Williams, Paul
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1647, Issue 1-2
  • DOI: 10.1016/S1570-9639(03)00042-6

Three-Dimensional Structure Determination of a Protein Supercomplex That Oxidizes Methane to Formaldehyde in Methylococcus capsulatus (Bath)
journal, October 2006

  • Myronova, Natalia; Kitmitto, Ashraf; Collins, Richard F.
  • Biochemistry, Vol. 45, Issue 39
  • DOI: 10.1021/bi061294p

The tungsten-containing formate dehydrogenase from Methylobacterium extorquens AM1: Purification and properties
journal, January 2003


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
  • DOI: 10.1007/BF02346062

Methanobactins: Maintaining copper homeostasis in methanotrophs and beyond
journal, January 2018

  • Kenney, Grace E.; Rosenzweig, Amy C.
  • Journal of Biological Chemistry, Vol. 293, Issue 13
  • DOI: 10.1074/jbc.TM117.000185

Structure and Protein–Protein Interactions of Methanol Dehydrogenase from Methylococcus capsulatus (Bath)
journal, September 2014

  • Culpepper, Megen A.; Rosenzweig, Amy C.
  • Biochemistry, Vol. 53, Issue 39
  • DOI: 10.1021/bi500850j

Differential expression analysis for sequence count data
journal, October 2010


The primary structure of cytochrome P460 of Nitrosomonas europaea : Presence of a c -heme binding motif
journal, October 1994


TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013


DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra
journal, February 2008


Methanobactin and the Link between Copper and Bacterial Methane Oxidation
journal, March 2016

  • DiSpirito, Alan A.; Semrau, Jeremy D.; Murrell, J. Colin
  • Microbiology and Molecular Biology Reviews, Vol. 80, Issue 2
  • DOI: 10.1128/MMBR.00058-15

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Methane utilization in Methylomicrobium alcaliphilum 20ZR: a systems approach
journal, February 2018


Trace Metal Requirements for Microbial Enzymes Involved in the Production and Consumption of Methane and Nitrous Oxide
journal, January 2012


Cerium Regulates Expression of Alternative Methanol Dehydrogenases in Methylosinus trichosporium OB3b
journal, August 2015

  • Farhan Ul Haque, Muhammad; Kalidass, Bhagyalakshmi; Bandow, Nathan
  • Applied and Environmental Microbiology, Vol. 81, Issue 21
  • DOI: 10.1128/AEM.02542-15

Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited
journal, March 2011


Current Trends in Methylotrophy
journal, August 2018


Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition
journal, December 2000


A Catalytic Role of XoxF1 as La3+-Dependent Methanol Dehydrogenase in Methylobacterium extorquens Strain AM1
journal, November 2012


Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
journal, March 2018


Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans
journal, May 2011

  • Hibi, Yoshihisa; Asai, Kentaro; Arafuka, Hiroshi
  • Journal of Bioscience and Bioengineering, Vol. 111, Issue 5
  • DOI: 10.1016/j.jbiosc.2010.12.017

Genome Sequence of the Haloalkaliphilic Methanotrophic Bacterium Methylomicrobium alcaliphilum 20Z
journal, December 2011

  • Vuilleumier, S.; Khmelenina, V. N.; Bringel, F.
  • Journal of Bacteriology, Vol. 194, Issue 2
  • DOI: 10.1128/JB.06392-11

Oxidation of hydroxylamine by cytochrome P-460 of the obligate methylotroph Methylococcus capsulatus Bath.
journal, October 1994


C1-Pathways in Methyloversatilis universalis FAM5: Genome Wide Gene Expression and Mutagenesis Studies
journal, April 2015


Genes essential for phototrophic growth by a purple alphaproteobacterium: Genes for phototrophic growth
journal, July 2017

  • Yang, Jianming; Yin, Liang; Lessner, Faith H.
  • Environmental Microbiology, Vol. 19, Issue 9
  • DOI: 10.1111/1462-2920.13852

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
  • DOI: 10.1111/1462-2920.12249

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
  • DOI: 10.1007/s00253-014-5766-8

Lanthanide-Dependent Regulation of Methylotrophy in Methylobacterium aquaticum Strain 22A
journal, January 2018


Metals and Methanotrophy
journal, January 2018

  • Semrau, Jeremy D.; DiSpirito, Alan A.; Gu, Wenyu
  • Applied and Environmental Microbiology, Vol. 84, Issue 6
  • DOI: 10.1128/AEM.02289-17

CorA Is a Copper Repressible Surface-Associated Copper(I)-Binding Protein Produced in Methylomicrobium album BG8
journal, February 2014


De novo assembly of bacterial transcriptomes from RNA-seq data
journal, January 2015


Molecular structure and gene analysis of Ce3+-induced methanol dehydrogenase of Bradyrhizobium sp. MAFF211645
journal, June 2011

  • Fitriyanto, Nanung Agus; Fushimi, Mako; Matsunaga, Mika
  • Journal of Bioscience and Bioengineering, Vol. 111, Issue 6
  • DOI: 10.1016/j.jbiosc.2011.01.015

Copper and cerium-regulated gene expression in Methylosinus trichosporium OB3b
journal, October 2017


HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014


Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission
journal, November 2016

  • Caranto, Jonathan D.; Vilbert, Avery C.; Lancaster, Kyle M.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 51
  • DOI: 10.1073/pnas.1611051113

Three decades of global methane sources and sinks
journal, September 2013

  • Kirschke, Stefanie; Bousquet, Philippe; Ciais, Philippe
  • Nature Geoscience, Vol. 6, Issue 10
  • DOI: 10.1038/ngeo1955

Universal sample preparation method for proteome analysis
journal, April 2009

  • Wiśniewski, Jacek R.; Zougman, Alexandre; Nagaraj, Nagarjuna
  • Nature Methods, Vol. 6, Issue 5
  • DOI: 10.1038/nmeth.1322

Role of copper and iron in methane oxidation and bacterial biopolymer accumulation
journal, February 2015

  • Chidambarampadmavathy, Karthigeyan; Obulisamy P., Karthikeyan; Heimann, Kirsten
  • Engineering in Life Sciences, Vol. 15, Issue 4
  • DOI: 10.1002/elsc.201400127

Multiple Formate Dehydrogenase Enzymes in the Facultative Methylotroph Methylobacterium extorquens AM1 Are Dispensable for Growth on Methanol
journal, December 2003


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
  • DOI: 10.1128/JB.00937-15

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
  • DOI: 10.7717/peerj.2435

Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1)
journal, November 2015

  • de la Torre, Andrea; Metivier, Aisha; Chu, Frances
  • Microbial Cell Factories, Vol. 14, Issue 1
  • DOI: 10.1186/s12934-015-0377-3

Functional investigation of methanol dehydrogenase-like protein XoxF in Methylobacterium extorquens AM1
journal, May 2010


Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis
journal, May 2002

  • Gupta, Rajeev; He, Zengyong; Luan, Sheng
  • Nature, Vol. 417, Issue 6888
  • DOI: 10.1038/417567a

The Sequence Alignment/Map format and SAMtools
journal, June 2009


MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014

  • Kim, Sangtae; Pevzner, Pavel A.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6277

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.