Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes.
Endosymbiotic theory in eukaryotic-cell evolution rests upon a foundation of three cornerstone partners--the plastid (a cyanobacterium), the mitochondrion (a proteobacterium), and its host (an archaeon)--and carries a corollary that, over time, the majority of genes once present in the organelle genomes were relinquished to the chromosomes of the host (endosymbiotic gene transfer). However, notwithstanding eukaryote-specific gene inventions, single-gene phylogenies have never traced eukaryotic genes to three single prokaryotic sources, an issue that hinges crucially upon factors influencing phylogenetic inference. In the age of genomes, single-gene trees, once used to test the predictions of endosymbiotic theory, now spawn new theories that stand to eventually replace endosymbiotic theory with descriptive, gene tree-based variants featuring supernumerary symbionts: prokaryotic partners distinct from the cornerstone trio and whose existence is inferred solely from single-gene trees. We reason that the endosymbiotic ancestors of mitochondria and chloroplasts brought into the eukaryotic--and plant and algal--lineage a genome-sized sample of genes from the proteobacterial and cyanobacterial pangenomes of their respective day and that, even if molecular phylogeny were artifact-free, sampling prokaryotic pangenomes through endosymbiotic gene transfer would lead to inherited chimerism. Recombination in prokaryotes (transduction, conjugation, transformation) differs from recombination in eukaryotes (sex). Prokaryotic recombination leads to pangenomes, and eukaryotic recombination leads to vertical inheritance. Viewed from the perspective of endosymbiotic theory, the critical transition at the eukaryote origin that allowed escape from Muller's ratchet--the origin of eukaryotic recombination, or sex--might have required surprisingly little evolutionary innovation.
Institute of Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; and.
Chuan
C
Ku
Institute of Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; and.
Shijulal
S
Nelson-Sathi
Institute of Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; and.
Mayo
M
Roettger
Institute of Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; and.
Sriram
S
Garg
Department of Natural and Life Sciences, The Open University of Israel, Ra'anana 43107, Israel.
Einat
E
Hazkani-Covo
Institute of Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; and bill@hhu.de.
William F
WF
Martin
D000483:Alleles; D000818:Animals; D002736:Chloroplasts / Q000235:genetics; D019295:Computational Biology; D000458:Cyanobacteria / Q000235:genetics; D004269:DNA, Bacterial / Q000235:genetics; D004926:Escherichia coli / Q000235:genetics; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D016678:Genome; D016680:Genome, Bacterial; D006801:Humans; D008928:Mitochondria / Q000235:genetics; D010802:Phylogeny; D018087:Plastids / Q000235:genetics; D011995:Recombination, Genetic; D013559:Symbiosis / Q000235:genetics*
D004269:DNA, Bacterial
endosymbiosis; evolution; lateral gene transfer; mitochondria; plastids