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

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 ? proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic ? 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 ? 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 ? 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 ? 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.

SUBMITTER: Degli Esposti M

PROVIDER: S-EPMC4967309 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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

Degli Esposti Mauro M Cortez Diego D Lozano Luis L Rasmussen Simon S Nielsen Henrik Bjørn HB Martinez Romero Esperanza E

Biology direct 20160730

<h4>Unlabelled</h4>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 mitochondri ...[more]

PMID: 27473689

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Project description:Several bacterial and archaeal lineages produce nanostructures that morphologically resemble small tailed viruses, but, unlike most viruses, contain apparently random pieces of the host genome. Since these elements can deliver the packaged DNA to other cells, they were dubbed gene transfer agents (GTAs). Because many genes involved in GTA production have viral homologs, it has been hypothesized that the GTA ancestor was a virus. Whether GTAs represent an atypical virus, a defective virus, or a virus co-opted by the prokaryotes for some function, remains to be elucidated. To evaluate these possibilities, we examined the distribution and evolutionary histories of genes that encode a GTA in the α-proteobacterium Rhodobacter capsulatus (RcGTA). We report that although homologs of many individual RcGTA genes are abundant across bacteria and their viruses, RcGTA-like genomes are mainly found in one subclade of α-proteobacteria. When compared with the viral homologs, genes of the RcGTA-like genomes evolve significantly slower, and do not have higher %A+T nucleotides than their host chromosomes. Moreover, they appear to reside in stable regions of the bacterial chromosomes that are generally conserved across taxonomic orders. These findings argue against RcGTA being an atypical or a defective virus. Our phylogenetic analyses suggest that RcGTA ancestor likely originated in the lineage that gave rise to contemporary α-proteobacterial orders Rhizobiales, Rhodobacterales, Caulobacterales, Parvularculales, and Sphingomonadales, and since that time the RcGTA-like element has co-evolved with its host chromosomes. Such evolutionary history is compatible with maintenance of these elements by bacteria due to some selective advantage. As for many other prokaryotic traits, horizontal gene transfer played a substantial role in the evolution of RcGTA-like elements, not only in shaping its genome components within the orders, but also in occasional dissemination of RcGTA-like regions across the orders and even to different bacterial phyla.

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

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

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