Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR
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 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) expressionmore »
- Authors:
-
- San Diego State Univ., San Diego, CA (United States); Institute of Cytology and Genetics SB RAS, Novosibirsk (Russia); Novosibirsk State University (Russia)
- San Diego State Univ., San Diego, CA (United States)
- Institute of Cytology and Genetics SB RAS, Novosibirsk (Russia)
- 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)
- OSTI Identifier:
- 1507987
- Report Number(s):
- PNNL-SA-139645
Journal ID: ISSN 1664-302X
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Journal Article: 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. https://doi.org/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. 2018.
"Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR". United States. https://doi.org/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},
url = {https://www.osti.gov/biblio/1507987},
journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 9,
place = {United States},
year = {Tue Nov 27 00:00:00 EST 2018},
month = {Tue Nov 27 00:00:00 EST 2018}
}
Web of Science
Figures / Tables:
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Figures / Tables found in this record: