Abstract
The ancestors of mitochondria, or proto-mitochondria, played a crucial role in the evolution of eukaryotic cells and derived from symbiotic α-proteobacteria which merged with other microorganisms - the basis of the widely accepted endosymbiotic theory. However, the identity and relatives of proto-mitochondria remain elusive. Here we show that methylotrophic α-proteobacteria could be the closest living models for mitochondrial ancestors. We reached this conclusion after reconstructing the possible evolutionary pathways of the bioenergy systems of proto-mitochondria with a genomic survey of extant α-proteobacteria. Results obtained with complementary molecular and genetic analyses of diverse bioenergetic proteins converge in indicating the pathway stemming from methylotrophic bacteria as the most probable route of mitochondrial evolution. Contrary to other α-proteobacteria, methylotrophs show transition forms for the bioenergetic systems analysed. Our approach of focusing on these bioenergetic systems overcomes the phylogenetic impasse that has previously complicated the search for mitochondrial ancestors. Moreover, our results provide a new perspective for experimentally re-evolving mitochondria from extant bacteria and in the future produce synthetic mitochondria.
Highlights
A major concept in biology is that the evolution of eukaryotic cell followed a symbiotic event between diverse microorganisms [1,2,3,4]
It is generally assumed that proto-mitochondria had an aerobic energy metabolism equivalent to that of today’s mitochondria [1,4,12], with the central part of the respiratory chain consisting of ubiquinol-cytochrome c reductase and a single terminal oxidase, cytochrome aa3 oxidase (Fig. 1A)
Rather than taking into consideration all the information that is available from bacterial and mitochondrial genomes, we have focused on a few proteins that are crucial for bioenergy production in both bacteria and mitochondria and have multiple variants
Summary
A major concept in biology is that the evolution of eukaryotic cell followed a symbiotic event between diverse microorganisms [1,2,3,4]. The reconstruction of proto-mitochondrial metabolism [12] has been partially contradicted by recent evidence suggesting that proto-mitochondria could be related to facultatively anaerobic generalists such as Rhodobacter [6,7,8,10] - which are capable of anoxygenic photosynthesis, an autotrophic function that must have been lost early along the evolution of mitochondria This evidence has recently been challenged by controversial reports that aerobic marine organisms such as Pelagibacter ubique may be the closest living relatives of mitochondria [13,14,15]. The wide diversity of the proposed bacterial ancestors of mitochondria arises from the different approaches of molecular evolution that have been used and the inherent limits of such approaches [1,2,3,4]
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