Endosymbiotic origin and differential loss of eukaryotic genes

Chuan Ku, Shijulal Nelson-Sathi, Mayo Roettger, Filipa L. Sousa, Peter J. Lockhart, David Bryant, Einat Hazkani-Covo, James O. McInerney, Giddy Landan and William F. Martin ()
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Chuan Ku: Institute of Molecular Evolution, Heinrich-Heine University
Shijulal Nelson-Sathi: Institute of Molecular Evolution, Heinrich-Heine University
Mayo Roettger: Institute of Molecular Evolution, Heinrich-Heine University
Filipa L. Sousa: Institute of Molecular Evolution, Heinrich-Heine University
Peter J. Lockhart: Institute of Fundamental Sciences, Massey University
David Bryant: University of Otago
Einat Hazkani-Covo: The Open University of Israel
James O. McInerney: National University of Ireland
Giddy Landan: Genomic Microbiology Group, Institute of Microbiology, Christian-Albrechts-University of Kiel
William F. Martin: Institute of Molecular Evolution, Heinrich-Heine University

Nature, 2015, vol. 524, issue 7566, 427-432

Abstract: Abstract Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. Here we discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. Our results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to long-term gene content evolution in eukaryotic genomes.

Date: 2015
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DOI: 10.1038/nature14963

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