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

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…We note that the "shopping bag" hypothesis (79), which argues that establishment of an endosymbiosis should be regarded as a continuous process involving a number of partners rather than a single event involving two partners, fits our data remarkably well. Of course, our data do not rule out inherited chimerism as a contributor to the taxonomic diversity of genes that support organelle function, because many bacterial genomes are taxonomically mosaic because of HGT (73). As with most solutions to endosymbiotic problems, the true answer is likely a complicated mixture of both processes.…”

“…The textbook concept is that a bacterium was taken up by a host cell, transferred most of its genes, and became the mitochondrion or plastid (70). This idea becomes more complicated when the taxonomic affiliation of bacterial genes on eukaryotic genomes is examined (71)(72)(73)(74). For example, only about 20% of mitochondria-related horizontally transferred genes have strong α-proteobacterial phylogenetic affinities (72).…”

“…Others favor a more abrupt "mitochondria early" scenario, where an endosymbiont with a taxonomically diverse mosaic genome made the transition to becoming the mitochondrion in a single endosymbiotic event, transferring its genes during the process. In this scenario, the mosaic nature of the extant eukaryotic genomes resulted from the "inherited chimerism" of the lone mitochondria bacterial ancestor because of the propensity of bacteria to participate in HGT with distantly related groups (73,77,78).…”

Horizontal gene flow from Eubacteria to Archaebacteria and what it means for our understanding of eukaryogenesis

“…This might be because HGT-based prokaryotic recombination, as opposed to sex-based eukaryotic recombination, leads to chimeric pangenomes where individual genes frequently have different phylogenetic histories. That is, the eubacterial partners in these putative, ancient, hybridization events would have been chimerical organisms to start with [38,39].…”

Symbiosis becoming permanent: Survival of the luckiest

“…The colloquium was a collaboration between the US National Academy of Sciences and the Canadian Institute for Advanced Research, and spanned a wide range of overlapping themes in symbiosis: major evolutionary transitions and the nature of individuality (10-13); the mosaic phylogenetic nature of organelle proteomes (14)(15)(16)(17); the risks and costs associated with long-term endosymbiosis (18,19); the structure and dynamics of symbiont and organelle genomes (20)(21)(22); the metabolic complexities that develop during the establishment and integration of endosymbionts (23-31); and how endosymbiosis has been understood in the history of biology and how it might be thought of in the future (32,33).…”