Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT

Abstract Ferroplasmaceae represent ubiquitous iron-oxidising extreme acidophiles with a number of unique physiological traits. In a genome-based study of Ferroplasma acidiphilum YT, the only species of the genus Ferroplasma with a validly published name, we assessed its central metabolism and genome...

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Autores principales: Olga V. Golyshina, Hai Tran, Oleg N. Reva, Sofia Lemak, Alexander F. Yakunin, Alexander Goesmann, Taras Y. Nechitaylo, Violetta LaCono, Francesco Smedile, Alexei Slesarev, David Rojo, Coral Barbas, Manuel Ferrer, Michail M. Yakimov, Peter N. Golyshin
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Publicado: Nature Portfolio 2017
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spelling oai:doaj.org-article:629dac02ca6a479a8117a205e987ca692021-12-02T12:32:55ZMetabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT10.1038/s41598-017-03904-52045-2322https://doaj.org/article/629dac02ca6a479a8117a205e987ca692017-06-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-03904-5https://doaj.org/toc/2045-2322Abstract Ferroplasmaceae represent ubiquitous iron-oxidising extreme acidophiles with a number of unique physiological traits. In a genome-based study of Ferroplasma acidiphilum YT, the only species of the genus Ferroplasma with a validly published name, we assessed its central metabolism and genome stability during a long-term cultivation experiment. Consistently with physiology, the genome analysis points to F. acidiphilum YT having an obligate peptidolytic oligotrophic lifestyle alongside with anaplerotic carbon assimilation. This narrow trophic specialisation abridges the sugar uptake, although all genes for glycolysis and gluconeogenesis, including bifunctional unidirectional fructose 1,6-bisphosphate aldolase/phosphatase, have been identified. Pyruvate and 2-oxoglutarate dehydrogenases are substituted by ‘ancient’ CoA-dependent pyruvate and alpha-ketoglutarate ferredoxin oxidoreductases. In the lab culture, after ~550 generations, the strain exhibited the mutation rate of ≥1.3 × 10−8 single nucleotide substitutions per site per generation, which is among the highest values recorded for unicellular organisms. All but one base substitutions were G:C to A:T, their distribution between coding and non-coding regions and synonymous-to-non-synonymous mutation ratios suggest the neutral drift being a prevalent mode in genome evolution in the lab culture. Mutations in nature seem to occur with lower frequencies, as suggested by a remarkable genomic conservation in F. acidiphilum YT variants from geographically distant populations.Olga V. GolyshinaHai TranOleg N. RevaSofia LemakAlexander F. YakuninAlexander GoesmannTaras Y. NechitayloVioletta LaConoFrancesco SmedileAlexei SlesarevDavid RojoCoral BarbasManuel FerrerMichail M. YakimovPeter N. GolyshinNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-12 (2017)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Olga V. Golyshina
Hai Tran
Oleg N. Reva
Sofia Lemak
Alexander F. Yakunin
Alexander Goesmann
Taras Y. Nechitaylo
Violetta LaCono
Francesco Smedile
Alexei Slesarev
David Rojo
Coral Barbas
Manuel Ferrer
Michail M. Yakimov
Peter N. Golyshin
Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
description Abstract Ferroplasmaceae represent ubiquitous iron-oxidising extreme acidophiles with a number of unique physiological traits. In a genome-based study of Ferroplasma acidiphilum YT, the only species of the genus Ferroplasma with a validly published name, we assessed its central metabolism and genome stability during a long-term cultivation experiment. Consistently with physiology, the genome analysis points to F. acidiphilum YT having an obligate peptidolytic oligotrophic lifestyle alongside with anaplerotic carbon assimilation. This narrow trophic specialisation abridges the sugar uptake, although all genes for glycolysis and gluconeogenesis, including bifunctional unidirectional fructose 1,6-bisphosphate aldolase/phosphatase, have been identified. Pyruvate and 2-oxoglutarate dehydrogenases are substituted by ‘ancient’ CoA-dependent pyruvate and alpha-ketoglutarate ferredoxin oxidoreductases. In the lab culture, after ~550 generations, the strain exhibited the mutation rate of ≥1.3 × 10−8 single nucleotide substitutions per site per generation, which is among the highest values recorded for unicellular organisms. All but one base substitutions were G:C to A:T, their distribution between coding and non-coding regions and synonymous-to-non-synonymous mutation ratios suggest the neutral drift being a prevalent mode in genome evolution in the lab culture. Mutations in nature seem to occur with lower frequencies, as suggested by a remarkable genomic conservation in F. acidiphilum YT variants from geographically distant populations.
format article
author Olga V. Golyshina
Hai Tran
Oleg N. Reva
Sofia Lemak
Alexander F. Yakunin
Alexander Goesmann
Taras Y. Nechitaylo
Violetta LaCono
Francesco Smedile
Alexei Slesarev
David Rojo
Coral Barbas
Manuel Ferrer
Michail M. Yakimov
Peter N. Golyshin
author_facet Olga V. Golyshina
Hai Tran
Oleg N. Reva
Sofia Lemak
Alexander F. Yakunin
Alexander Goesmann
Taras Y. Nechitaylo
Violetta LaCono
Francesco Smedile
Alexei Slesarev
David Rojo
Coral Barbas
Manuel Ferrer
Michail M. Yakimov
Peter N. Golyshin
author_sort Olga V. Golyshina
title Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
title_short Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
title_full Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
title_fullStr Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
title_full_unstemmed Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT
title_sort metabolic and evolutionary patterns in the extremely acidophilic archaeon ferroplasma acidiphilum yt
publisher Nature Portfolio
publishDate 2017
url https://doaj.org/article/629dac02ca6a479a8117a205e987ca69
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