Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes

Abstract

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.

Keywords: endosymbiosis; evolution; lateral gene transfer; mitochondria; plastids.

Fig. 1.

Recombination and inheritance in prokaryotes and eukaryotes. (A) Gene transfer in prokaryotes leads to new genes in different clonally propagating lines. Gene gain (colored segments) is counterbalanced by differential loss. (B) Recombination and gamete fusion in eukaryotes (highly schematic) lead to vertically evolving lineages.

Fig. 2.

Bacterial pangenome distribution. The bidirectional best BLAST hit approach (63) was performed on protein sequences of 1,981 complete prokaryotic genomes [see Nelson-Sathi et al. (64) for the full list] that had hits with ≥25% local identity and e-value <10⁻¹⁰ in BLAST (65) search. Grouping into protein families was performed using the Markov Chain clustering procedure (66). Patterns of presence (black) and absence (white) of all protein-coding genes are shown. Each genome is represented by a row and gene families by columns. Gene families are sorted in decreasing order (left to right) of their presence in the total genomes. The core genes are shown on the left side and genome-specific genes to the right. (A) Distribution of 16,725 genes in 54 E. coli genomes, with 8,776 (52.5%) clusters present in at least two genomes and 7,949 (47.5%) unique to individual strains (singletons). Among the singletons, 1,132 genes have at least one homolog in non-E. coli species. (B) Distribution of 33,118 genes in 44 cyanobacterial genomes, including 12,236 found in at least two genomes and 20,882 singletons. (C) A total of 96,916 genes are present in 208 alphaproteobacterial genomes, including 36,176 in at least 2 genomes and 60,740 singletons.

Fig. 3.

Gene sharing among prokaryotes. (A, Upper) Presence/absence of protein families in cyanobacterial genomes, sorted according to the number of taxonomic groups sharing the corresponding gene. (Lower) Proportion of genes in each cyanobacterial genome shared with other taxonomic groups. k-means clustering was applied to sort taxonomic groups according to pattern similarity. (B) Showing the same patterns as in A for alphaproteobacteria. (Lower) Taxonomic groups are sorted as in A. This figure is based on the nonsingleton clusters from those described in Fig. 2. For the complete figure with taxon labels, see Fig. S1.

Fig. 4.

Histories hidden behind trees. (A) In an ideal tree of a gene acquired endosymbiotically from a donor prokaryotic lineage (green), eukaryotes (black) should be nested within present-day representatives of that lineage. (B) LGT among prokaryotes results in a prokaryotic sister group consisting of homologs from both donor and nondonor lineages (nongreen colors). Further complicated by gene loss (crosses) and incomplete sampling (only circled homologs are sampled and used for phylogenetic analyses), the sister group observed in the tree is an apparent one that is a subsample of the complete sister group (C) or does not contain any representative from the true sister group (D). (E) The same factors also influence sampling of eukaryotic homologs, resulting in an apparent acquisition of the gene by a subgroup of the eukaryotic clade involved in the endosymbiosis event.