Twist in the tail of eukaryotic origins
15:18 19 December 2011 by Wendy Zukerman
Complex life may have had parasitic origins. New evidence suggests that the relatives of the mitochondria within our cells once had a tail, like many parasitic bacteria.
Life on Earth is packaged into three domains: the simple bacteria, the archaea, and the complex eukaryotes that make up most of the life we see with the naked eye.
The first eukaryotes appeared around 2 billion years ago. One popular theory suggests they did so after an immobile bacterium was ingested by an archaeon. The bacterium somehow escaped being digested and instead formed a symbiotic relationship with its consumer. As that relationship blossomed, the engulfed bacteria evolved into mitochondria – the energy producers in our cells.
Different picture
Nathan Lo at the University of Sydney in Australia and Claudio Bandi at the University of Valencia in Spain think it is time to view this serendipitous encounter in a different light. They say that a few bacteria within the Rickettsiales – the closest genetic match to mitochondria – carry genes for a flagellum, a whip-like tail that some bacteria use to propel themselves.
That suggests that the bacteria might once have been mobile, like many parasitic bacteria. "Our results indicate that the mitochondrial ancestor may have acted as a parasite rather than prey," says Lo.
Lo and Bandi focused on Midichloria mitochondrii, a relatively little-known member of the Rickettsiales. Although the Rickettsiales do not boast a flagellum, the Midichloria genome contained 26 genes that help to build one in other bacteria. "We thought, that's strange," says Lo. "Where the hell did these genes come from?"
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Phylogenomic Evidence for the Presence of a Flagellum and cbb3Oxidase in the Free-Living Mitochondrial Ancestor
Davide Sassera†,1, Nathan Lo†,2, Sara Epis1, Giuseppe D'Auria3, Matteo Montagna1, Francesco Comandatore1, David Horner4, Juli Peretó3,5,6, Alberto Maria Luciano7, Federica Franciosi7,Emanuele Ferri8, Elena Crotti9, Chiara Bazzocchi1, Daniele Daffonchio9, Luciano Sacchi10, Andres Moya3,5,11, Amparo Latorre3,5,11 and Claudio Bandi1,*
Author Affiliations
1Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy
2School of Biological Sciences, The University of Sydney, Sydney, New South Wales, Australia
3Centro Superior de Investigación en Salud Pública, Generalitat Valenciana, Valencia, Spain
4Dipartimento di Scienze Biomolecolari e Biotecnologie, Università degli Studi di Milano, Milano, Italy
5Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, València, Spain
6Departament de Bioquímica i Biologia Molecular, Universitat de València, València, Spain
7Dipartimento di Scienze Animali, Università degli Studi di Milano, Milano, Italy
8Dipartimento di Biotecnologie e Bioscienze, Università degli Studi di Milano Bicocca, Milano, Italy
9Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche, Università degli Studi di Milano, Milano, Italy
10Dipartimento di Biologia Animale, Università degli Studi di Pavia, Pavia, Italy
11Departament de Genètica, Universitat de València, València, Spain
*Corresponding author: E-mail: claudio.bandi@unimi.it.
Abstract
The initiation of the intracellular symbiosis that would give rise to mitochondria and eukaryotes was a major event in the history of life on earth. Hypotheses to explain eukaryogenesis fall into two broad and competing categories: those proposing that the host was a phagocytotic proto-eukaryote that preyed upon the free-living mitochondrial ancestor (hereafter FMA), and those proposing that the host was an archaebacterium that engaged in syntrophy with the FMA. Of key importance to these hypotheses are whether the FMA was motile or nonmotile, and the atmospheric conditions under which the FMA thrived. Reconstructions of the FMA based on genome content of Rickettsiales representatives—generally considered to be the closest living relatives of mitochondria—indicate that it was nonmotile and aerobic. We have sequenced the genome ofCandidatus Midichloria mitochondrii, a novel and phylogenetically divergent member of the Rickettsiales. We found that it possesses unique gene sets found in no other Rickettsiales, including 26 genes associated with flagellar assembly, and a cbb3-type cytochrome oxidase. Phylogenomic analyses show that these genes were inherited in a vertical fashion from an ancestral α-proteobacterium, and indicate that the FMA possessed a flagellum, and could undergo oxidative phosphorylation under both aerobic and microoxic conditions. These results indicate that the FMA played a more active and potentially parasitic role in eukaryogenesis than currently appreciated and provide an explanation for how the symbiosis could have evolved under low levels of oxygen.
Key words: mitochondrion, symbiosis, eukaryogenesis, Midichloria mitochondrii, rickettsiales, phylogenomics
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