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

Mauro Degli Esposti,Luis Lozano,Diego Cortez,Simon Rasmussen,Henrik Bjørn Nielsen,Esperanza Martinez Romero

doi:10.1186/s13062-016-0136-3

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.Reviewers: This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-016-0136-3) contains supplementary material, which is available to authorized users.

Highlights

Mounting interest is arising on eukaryogenesis, a major transition in evolution which most likely originated from a symbiogenic event between an archaea and a metabolically versatile bacterium [1, 2]
Trichomonas, Entamoeba and other eukaryotes adapted to anaerobic conditions possess Mitochondria Related Organelles (MRO [3, 12,13,14]) carrying out reactions of anaerobic metabolism that are typical of obligate anaerobes such as Clostridium, rather than α proteobacteria [12,13,14,15,16,17,18,19]. [FeFe]-hydrogenase constitutes the distinctive enzyme of this anaerobic metabolism and is present in different types [12,13,14,15,16,17,18,19], both in MRO and the cytosol of anaerobic eukaryotes such as Mastigamoeba [18]
Contrary to established views that the anaerobic metabolism of eukaryotes might have been inherited through lateral gene transfer (LGT) phenomena from prokaryotes other than α proteobacteria [11, 12, 17, 18], we have shown here that a subset of α proteobacterial organisms of the Rhodospirillales order contain the two principal forms of eukaryotic [FeFe]-hydrogenases characteristic of this metabolism, and the maturases required for the assembly of such enzymes (Table 1, Fig. 2 and Additional file 1: Figure S1)

Summary

Introduction

Mounting interest is arising on eukaryogenesis, a major transition in evolution which most likely originated from a symbiogenic event between an archaea and a metabolically versatile bacterium [1, 2]. Recent analysis of major bioenergetic systems shared by bacteria and mitochondria suggests that a subset of extant α proteobacteria could be related to the ancestral lineage from which mitochondrial organelles of eukaryotic cells evolved [4, 8, 10]. Trichomonas, Entamoeba and other eukaryotes adapted to anaerobic conditions possess Mitochondria Related Organelles (MRO [3, 12,13,14]) carrying out reactions of anaerobic metabolism that are typical of obligate anaerobes such as Clostridium, rather than α proteobacteria [12,13,14,15,16,17,18,19]. The wide molecular variations of [FeFe]-hydrogenases [11, 12, 15,16,17,18,19] are present in many obligate anaerobes, in particular Clostridiales, Thermotogales and δ proteobacteria [12,13,14,15,16,17,18,19]; only a few facultative anaerobic α proteobacteria such as Rhodospirillum rubrum have similar

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Conclusion