Endosymbiotic origin and differential loss of eukaryotic genes.
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.
Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany.
Chuan
C
Ku
Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany.
Shijulal
S
Nelson-Sathi
Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany.
Mayo
M
Roettger
Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany.
Filipa L
FL
Sousa
Institute of Fundamental Sciences, Massey University, Palmerston North 4474, New Zealand.
Peter J
PJ
Lockhart
Department of Mathematics and Statistics, University of Otago, Dunedin 9054, New Zealand.
David
D
Bryant
Department of Natural and Life Sciences, The Open University of Israel, Ra'anana 43107, Israel.
Einat
E
Hazkani-Covo
Department of Biology, National University of Ireland, Maynooth, County Kildare, Ireland.|Michael Smith Building, The University of Manchester, Oxford Rd, Manchester M13 9PL, UK.
James O
JO
McInerney
Genomic Microbiology Group, Institute of Microbiology, Christian-Albrechts-University of Kiel, 24118 Kiel, Germany.
Giddy
G
Landan
Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany.|Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal.
William F
WF
Martin
D001105:Archaea / Q000235:genetics; D001419:Bacteria / Q000235:genetics; D016000:Cluster Analysis; D056890:Eukaryota / Q000145:classification / Q000235:genetics*; D005057:Eukaryotic Cells / Q000378:metabolism; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal / Q000235:genetics; D016678:Genome / Q000235:genetics; D008928:Mitochondria / Q000235:genetics; D008957:Models, Genetic; D015388:Organelles / Q000235:genetics*; D010802:Phylogeny; D018087:Plastids / Q000235:genetics; D011387:Prokaryotic Cells / Q000378:metabolism; D020543:Proteome / Q000235:genetics; D013559:Symbiosis / Q000235:genetics*; D013997:Time Factors
D020543:Proteome