Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions

ABSTRACT The ubiquitous ATP synthase uses an electrochemical gradient to synthesize cellular energy in the form of ATP. The production of this electrochemical gradient relies on liposoluble proton carriers like ubiquinone (UQ), which is used in the respiratory chains of eukaryotes and proteobacteria...

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Autores principales:	Ludovic Pelosi, Anne-Lise Ducluzeau, Laurent Loiseau, Frédéric Barras, Dominique Schneider, Ivan Junier, Fabien Pierrel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	biosynthesis evolution proteobacteria Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c79b886694bb46cb84e7b8a99f1eabad
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spelling	oai:doaj.org-article:c79b886694bb46cb84e7b8a99f1eabad2021-12-02T19:48:49ZEvolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions10.1128/mSystems.00091-162379-5077https://doaj.org/article/c79b886694bb46cb84e7b8a99f1eabad2016-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00091-16https://doaj.org/toc/2379-5077ABSTRACT The ubiquitous ATP synthase uses an electrochemical gradient to synthesize cellular energy in the form of ATP. The production of this electrochemical gradient relies on liposoluble proton carriers like ubiquinone (UQ), which is used in the respiratory chains of eukaryotes and proteobacteria. The biosynthesis of UQ requires three hydroxylation reactions on contiguous positions of an aromatic ring. In Escherichia coli, each of three UQ flavin monooxygenases (FMOs), called UbiF, UbiH, and UbiI, modifies a single position of the aromatic ring. This pattern of three hydroxylation reactions/three proteins has been accepted as a paradigm in UQ biology. Using a phylogenetic analysis, we found that UbiF, UbiH, and UbiI are detected only in a small fraction of proteobacteria, and we identified two new types of UQ FMOs: UbiM, which is distributed in members of the alpha, beta, and gamma classes of proteobacteria, and UbiL, which is restricted to members of the alphaproteobacteria. Remarkably, the ubiL and ubiM genes were found in genomes with fewer than three UQ hydroxylase-encoding genes. We demonstrated, using biochemical approaches, that UbiL from Rhodospirillum rubrum and UbiM from Neisseria meningitidis hydroxylate, respectively, two and three positions of the aromatic ring during UQ biosynthesis. We conclude that bacteria have evolved a large repertoire of hydroxylase combinations for UQ biosynthesis, including pathways with either three specialist enzymes or pathways with one or two generalist enzymes of broader regioselectivity. The emergence of the latter is potentially related to genome reduction events. IMPORTANCE UQ, a key molecule for cellular bioenergetics that is conserved from proteobacteria to humans, appeared in an ancestral proteobacterium more than 2 billion years ago. UQ biosynthesis has been studied only in a few model organisms, and thus, the diversity of UQ biosynthesis pathways is largely unknown. In the work reported here, we conducted a phylogenomic analysis of hydroxylases involved in UQ biosynthesis. Our results support the existence of at least two UQ hydroxylases in the proteobacterial ancestor, and yet, we show that their number varies from one to four in extant proteobacterial species. Our biochemical experiments demonstrated that bacteria containing only one or two UQ hydroxylases have developed generalist enzymes that are able to catalyze several steps of UQ biosynthesis. Our study documents a rare case where evolution favored the broadening of an enzyme’s regioselectivity, which resulted in gene loss in several proteobacterial species with small genomes.Ludovic PelosiAnne-Lise DucluzeauLaurent LoiseauFrédéric BarrasDominique SchneiderIvan JunierFabien PierrelAmerican Society for MicrobiologyarticlebiosynthesisevolutionproteobacteriaMicrobiologyQR1-502ENmSystems, Vol 1, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	biosynthesis evolution proteobacteria Microbiology QR1-502
spellingShingle	biosynthesis evolution proteobacteria Microbiology QR1-502 Ludovic Pelosi Anne-Lise Ducluzeau Laurent Loiseau Frédéric Barras Dominique Schneider Ivan Junier Fabien Pierrel Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
description	ABSTRACT The ubiquitous ATP synthase uses an electrochemical gradient to synthesize cellular energy in the form of ATP. The production of this electrochemical gradient relies on liposoluble proton carriers like ubiquinone (UQ), which is used in the respiratory chains of eukaryotes and proteobacteria. The biosynthesis of UQ requires three hydroxylation reactions on contiguous positions of an aromatic ring. In Escherichia coli, each of three UQ flavin monooxygenases (FMOs), called UbiF, UbiH, and UbiI, modifies a single position of the aromatic ring. This pattern of three hydroxylation reactions/three proteins has been accepted as a paradigm in UQ biology. Using a phylogenetic analysis, we found that UbiF, UbiH, and UbiI are detected only in a small fraction of proteobacteria, and we identified two new types of UQ FMOs: UbiM, which is distributed in members of the alpha, beta, and gamma classes of proteobacteria, and UbiL, which is restricted to members of the alphaproteobacteria. Remarkably, the ubiL and ubiM genes were found in genomes with fewer than three UQ hydroxylase-encoding genes. We demonstrated, using biochemical approaches, that UbiL from Rhodospirillum rubrum and UbiM from Neisseria meningitidis hydroxylate, respectively, two and three positions of the aromatic ring during UQ biosynthesis. We conclude that bacteria have evolved a large repertoire of hydroxylase combinations for UQ biosynthesis, including pathways with either three specialist enzymes or pathways with one or two generalist enzymes of broader regioselectivity. The emergence of the latter is potentially related to genome reduction events. IMPORTANCE UQ, a key molecule for cellular bioenergetics that is conserved from proteobacteria to humans, appeared in an ancestral proteobacterium more than 2 billion years ago. UQ biosynthesis has been studied only in a few model organisms, and thus, the diversity of UQ biosynthesis pathways is largely unknown. In the work reported here, we conducted a phylogenomic analysis of hydroxylases involved in UQ biosynthesis. Our results support the existence of at least two UQ hydroxylases in the proteobacterial ancestor, and yet, we show that their number varies from one to four in extant proteobacterial species. Our biochemical experiments demonstrated that bacteria containing only one or two UQ hydroxylases have developed generalist enzymes that are able to catalyze several steps of UQ biosynthesis. Our study documents a rare case where evolution favored the broadening of an enzyme’s regioselectivity, which resulted in gene loss in several proteobacterial species with small genomes.
format	article
author	Ludovic Pelosi Anne-Lise Ducluzeau Laurent Loiseau Frédéric Barras Dominique Schneider Ivan Junier Fabien Pierrel
author_facet	Ludovic Pelosi Anne-Lise Ducluzeau Laurent Loiseau Frédéric Barras Dominique Schneider Ivan Junier Fabien Pierrel
author_sort	Ludovic Pelosi
title	Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
title_short	Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
title_full	Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
title_fullStr	Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
title_full_unstemmed	Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions
title_sort	evolution of ubiquinone biosynthesis: multiple proteobacterial enzymes with various regioselectivities to catalyze three contiguous aromatic hydroxylation reactions
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/c79b886694bb46cb84e7b8a99f1eabad
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Evolution of Ubiquinone Biosynthesis: Multiple Proteobacterial Enzymes with Various Regioselectivities To Catalyze Three Contiguous Aromatic Hydroxylation Reactions

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