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

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 alcoh...

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Autores principales:	Yue Zheng, Jing Huang, Feng Zhao, Ludmila Chistoserdova
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	XoxG XoxF MxaFI MxaG Methylomonas methanol dehydrogenase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6d4bc3dd48884520b6334f485940c3dc
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spelling	oai:doaj.org-article:6d4bc3dd48884520b6334f485940c3dc2021-11-15T15:53:27ZPhysiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy10.1128/mBio.02430-172150-7511https://doaj.org/article/6d4bc3dd48884520b6334f485940c3dc2018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02430-17https://doaj.org/toc/2150-7511ABSTRACT 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.Yue ZhengJing HuangFeng ZhaoLudmila ChistoserdovaAmerican Society for MicrobiologyarticleXoxGXoxFMxaFIMxaGMethylomonasmethanol dehydrogenaseMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	XoxG XoxF MxaFI MxaG Methylomonas methanol dehydrogenase Microbiology QR1-502
spellingShingle	XoxG XoxF MxaFI MxaG Methylomonas methanol dehydrogenase Microbiology QR1-502 Yue Zheng Jing Huang Feng Zhao Ludmila Chistoserdova Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
description	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.
format	article
author	Yue Zheng Jing Huang Feng Zhao Ludmila Chistoserdova
author_facet	Yue Zheng Jing Huang Feng Zhao Ludmila Chistoserdova
author_sort	Yue Zheng
title	Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
title_short	Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
title_full	Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
title_fullStr	Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
title_full_unstemmed	Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy
title_sort	physiological effect of xoxg(4) on lanthanide-dependent methanotrophy
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/6d4bc3dd48884520b6334f485940c3dc
work_keys_str_mv	AT yuezheng physiologicaleffectofxoxg4onlanthanidedependentmethanotrophy AT jinghuang physiologicaleffectofxoxg4onlanthanidedependentmethanotrophy AT fengzhao physiologicaleffectofxoxg4onlanthanidedependentmethanotrophy AT ludmilachistoserdova physiologicaleffectofxoxg4onlanthanidedependentmethanotrophy
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Physiological Effect of XoxG(4) on Lanthanide-Dependent Methanotrophy

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