Alpha proteobacterial ancestry of the [Fe-Fe]-hydrogenases in anaerobic eukaryotes

Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The con...

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Published inBiology direct Vol. 11; no. 1; p. 34
Main Authors Degli Esposti, Mauro, Cortez, Diego, Lozano, Luis, Rasmussen, Simon, Nielsen, Henrik Bjørn, Martinez Romero, Esperanza
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 30.07.2016
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Abstract Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes. This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.
AbstractList Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba . These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes. Reviewers: This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.
Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to [alpha] proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic [alpha] proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than [alpha] proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that [alpha] proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an [alpha] proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes.
Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to [alpha] proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic [alpha] proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than [alpha] proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that [alpha] proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an [alpha] proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes. Reviewers: This article was reviewed by William Martin and Nick Lane, both suggested by the Authors. Keywords: Eukaryogenesis, Anaerobic metabolism, [FeFe]-hydrogenase, Mitochondria, Bioenergetics
UNLABELLEDEukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes.REVIEWERSThis article was reviewed by William Martin and Nick Lane, both suggested by the Authors.
Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes. This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.
ArticleNumber 34
Audience Academic
Author Lozano, Luis
Cortez, Diego
Rasmussen, Simon
Martinez Romero, Esperanza
Degli Esposti, Mauro
Nielsen, Henrik Bjørn
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Issue 1
Keywords Anaerobic metabolism
Mitochondria
Bioenergetics
[FeFe]-hydrogenase
Eukaryogenesis
Language English
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Snippet Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By...
UNLABELLEDEukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile...
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StartPage 34
SubjectTerms Alphaproteobacteria - genetics
Amino Acid Sequence
Bacterial Proteins - genetics
Discovery Notes
Eukaryotes
Evolution, Molecular
Gastrointestinal Microbiome - genetics
Humans
Hydrogenase - genetics
Phylogeny
Physiological aspects
Proteobacteria
Rhodospirillaceae - genetics
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Title Alpha proteobacterial ancestry of the [Fe-Fe]-hydrogenases in anaerobic eukaryotes
URI https://www.ncbi.nlm.nih.gov/pubmed/27473689
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https://pubmed.ncbi.nlm.nih.gov/PMC4967309
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