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Title: Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy

Abstract

ABSTRACT A recent surprising discovery of the activity of rare earth metals (lanthanides) as enzyme cofactors as well as transcriptional regulators has overturned the traditional assumption of biological inertia of these metals. However, so far, examples of such activities have been limited to alcohol dehydrogenases. Here we describe the physiological effects of a mutation in xoxG , a gene encoding a novel cytochrome, XoxG(4), and compare these to the effects of mutation in XoxF, a lanthanide-dependent methanol dehydrogenase, at the enzyme activity level and also at the community function level, using Methylomonas sp. strain LW13 as a model organism. Through comparative phenotypic characterization, we establish XoxG as the second protein directly involved in lanthanide-dependent metabolism, likely as a dedicated electron acceptor from XoxF. However, mutation in XoxG caused a phenotype that was dramatically different from the phenotype of the mutant in XoxF, suggesting a secondary function for this cytochrome, in metabolism of methane. We also purify XoxG(4) and demonstrate that this protein is a true cytochrome c , based on the typical absorption spectra, and we demonstrate that XoxG can be directly reduced by a purified XoxF, supporting one of its proposed physiological functions. Overall, our data continue to suggestmore » the complex nature of the interplay between the calcium-dependent and lanthanide-dependent alcohol oxidation systems, while they also suggest that addressing the roles of these alternative systems is essential at the enzyme and community function level, in addition to the gene transcription level. IMPORTANCE The lanthanide-dependent biochemistry of living organisms remains a barely tapped area of knowledge. So far, only a handful of lanthanide-dependent alcohol dehydrogenases have been described, and their regulation by lanthanides has been demonstrated at the transcription level. Little information is available regarding the concentrations of lanthanides that could support sufficient enzymatic activities to support specific metabolisms, and so far, no other redox proteins involved in lanthanide-dependent methanotrophy have been demonstrated. The research presented here provides enzyme activity-level data on lanthanide-dependent methanotrophy in a model methanotroph. Additionally, we identify a second protein important for lanthanide-dependent metabolism in this organism, XoxG(4), a novel cytochrome. XoxG(4) appears to have multiple functions in methanotrophy, one function as an electron acceptor from XoxF and another function remaining unknown. On the basis of the dramatic phenotype of the XoxG(4) mutant, this function must be crucial for methanotrophy.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Univ. of Washington, Seattle, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1429552
Alternate Identifier(s):
OSTI ID: 1510496
Grant/Contract Number:  
SC-0016224; SC0016224
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 9 Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 36 MATERIALS SCIENCE; XoxG; XoxF; MxaFI; MxaG; Methylomonas; methanol dehydrogenase

Citation Formats

Zheng, Yue, Huang, Jing, Zhao, Feng, Chistoserdova, Ludmila, and Giovannoni, ed., Stephen. Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy. United States: N. p., 2018. Web. doi:10.1128/mBio.02430-17.
Zheng, Yue, Huang, Jing, Zhao, Feng, Chistoserdova, Ludmila, & Giovannoni, ed., Stephen. Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy. United States. doi:10.1128/mBio.02430-17.
Zheng, Yue, Huang, Jing, Zhao, Feng, Chistoserdova, Ludmila, and Giovannoni, ed., Stephen. Tue . "Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy". United States. doi:10.1128/mBio.02430-17.
@article{osti_1429552,
title = {Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy},
author = {Zheng, Yue and Huang, Jing and Zhao, Feng and Chistoserdova, Ludmila and Giovannoni, ed., Stephen},
abstractNote = {ABSTRACT A recent surprising discovery of the activity of rare earth metals (lanthanides) as enzyme cofactors as well as transcriptional regulators has overturned the traditional assumption of biological inertia of these metals. However, so far, examples of such activities have been limited to alcohol dehydrogenases. Here we describe the physiological effects of a mutation in xoxG , a gene encoding a novel cytochrome, XoxG(4), and compare these to the effects of mutation in XoxF, a lanthanide-dependent methanol dehydrogenase, at the enzyme activity level and also at the community function level, using Methylomonas sp. strain LW13 as a model organism. Through comparative phenotypic characterization, we establish XoxG as the second protein directly involved in lanthanide-dependent metabolism, likely as a dedicated electron acceptor from XoxF. However, mutation in XoxG caused a phenotype that was dramatically different from the phenotype of the mutant in XoxF, suggesting a secondary function for this cytochrome, in metabolism of methane. We also purify XoxG(4) and demonstrate that this protein is a true cytochrome c , based on the typical absorption spectra, and we demonstrate that XoxG can be directly reduced by a purified XoxF, supporting one of its proposed physiological functions. Overall, our data continue to suggest the complex nature of the interplay between the calcium-dependent and lanthanide-dependent alcohol oxidation systems, while they also suggest that addressing the roles of these alternative systems is essential at the enzyme and community function level, in addition to the gene transcription level. IMPORTANCE The lanthanide-dependent biochemistry of living organisms remains a barely tapped area of knowledge. So far, only a handful of lanthanide-dependent alcohol dehydrogenases have been described, and their regulation by lanthanides has been demonstrated at the transcription level. Little information is available regarding the concentrations of lanthanides that could support sufficient enzymatic activities to support specific metabolisms, and so far, no other redox proteins involved in lanthanide-dependent methanotrophy have been demonstrated. The research presented here provides enzyme activity-level data on lanthanide-dependent methanotrophy in a model methanotroph. Additionally, we identify a second protein important for lanthanide-dependent metabolism in this organism, XoxG(4), a novel cytochrome. XoxG(4) appears to have multiple functions in methanotrophy, one function as an electron acceptor from XoxF and another function remaining unknown. On the basis of the dramatic phenotype of the XoxG(4) mutant, this function must be crucial for methanotrophy.},
doi = {10.1128/mBio.02430-17},
journal = {mBio (Online)},
number = 2,
volume = 9,
place = {United States},
year = {2018},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1128/mBio.02430-17

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    Works referencing / citing this record:

    Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR
    journal, November 2018

    • Akberdin, Ilya R.; Collins, David A.; Hamilton, Richard
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