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.

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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.endosymbiosis | evolution | mitochondria | lateral gene transfer | plastids

BackgroundThe literature harbors many claims for lateral gene transfer (LGT) from prokaryotes to eukaryotes. Such claims are typically founded in analyses of genome sequences. It is undisputed that many genes entered the eukaryotic lineage via the origin of mitochondria and the origin of plastids. Claims for lineage-specific LGT to eukaryotes outside the context of organelle origins and claims of continuous LGT to eukaryotic lineages are more problematic. If eukaryotes acquire genes from prokaryotes continuously during evolution, then sequenced eukaryote genomes should harbor evidence for recent LGT, like prokaryotic genomes do.ResultsHere we devise an approach to investigate 30,358 eukaryotic sequences in the context of 1,035,375 prokaryotic homologs among 2585 phylogenetic trees containing homologs from prokaryotes and eukaryotes. Prokaryote genomes reflect a continuous process of gene acquisition and inheritance, with abundant recent acquisitions showing 80–100 % amino acid sequence identity to their phylogenetic sister-group homologs from other phyla. By contrast, eukaryote genomes show no evidence for either continuous or recent gene acquisitions from prokaryotes. We find that, in general, genes in eukaryotic genomes that share ≥70 % amino acid identity to prokaryotic homologs are genome-specific; that is, they are not found outside individual genome assemblies.ConclusionsOur analyses indicate that eukaryotes do not acquire genes through continual LGT like prokaryotes do. We propose a 70 % rule: Coding sequences in eukaryotic genomes that share more than 70 % amino acid sequence identity to prokaryotic homologs are most likely assembly or annotation artifacts. The findings further uncover that the role of differential loss in eukaryote genome evolution has been vastly underestimated.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0315-9) contains supplementary material, which is available to authorized users.

Spiroplasma is a genus of wall-less, low-GC, Gram-positive bacteria with helical morphology. As commensals or pathogens of plants, insects, ticks, or crustaceans, they are closely related with mycoplasmas and form a monophyletic group (Spiroplasma–Entomoplasmataceae–Mycoides) with Mycoplasma mycoides and its relatives. In this study, we report the complete genome sequences of Spiroplasma chrysopicola and S. syrphidicola from the Chrysopicola clade. These species form the sister group to the Citri clade, which includes several well-known pathogenic spiroplasmas. Surprisingly, these two newly available genomes from the Chrysopicola clade contain no plectroviral genes, which were found to be highly repetitive in the previously sequenced genomes from the Citri clade. Based on the genome alignment and patterns of GC-skew, these two Chrysopicola genomes appear to be relatively stable, rather than being highly rearranged as those from the Citri clade. Phylogenetic analyses suggest that the susceptibility to plectroviral invasion probably originated in the common ancestor of the Citri clade or one of its subclades. This susceptibility may be attributed to the absence of antiviral systems found in the Chrysopicola clade. Using the virus-free genomes of the Chrysopicola clade as references, we inferred the putative viral integration sites in the Citri genomes. Comparisons of syntenic regions suggest that the extensive viral invasion in the Citri clade promoted genome rearrangements and expansions. More importantly, the viral invasion may have facilitated horizontal gene transfers that contributed to adaptation in the Citri clade.