Lateral gene transfer (LGT) has impacted prokaryotic genome evolution, yet the extent to which LGT compromises vertical evolution across individual genes and individual phyla is unknown, as are the factors that govern LGT frequency across genes. Estimating LGT frequency from tree comparisons is problematic when thousands of genomes are compared, because LGT becomes difficult to distinguish from phylogenetic artefacts. Here we report quantitative estimates for verticality across all genes and genomes, leveraging a well-known property of phylogenetic inference: phylogeny works best at the tips of trees. From terminal (tip) phylum level relationships, we calculate the verticality for 19,050,992 genes from 101,422 clusters in 5,655 prokaryotic genomes and rank them by their verticality. Among functional classes, translation, followed by nucleotide and cofactor biosynthesis, and DNA replication and repair are the most vertical. The most vertically evolving lineages are those rich in ecological specialists such as Acidithiobacilli, Chlamydiae, Chlorobi and Methanococcales. Lineages most affected by LGT are the α-, β-, γ-, and δ-classes of Proteobacteria and the Firmicutes. The 2,587 eukaryotic clusters in our sample having prokaryotic homologues fail to reject eukaryotic monophyly using the likelihood ratio test. The low verticality of α-proteobacterial and cyanobacterial genomes requires only three partners-an archaeal host, a mitochondrial symbiont, and a plastid ancestor-each with mosaic chromosomes, to directly account for the prokaryotic origin of eukaryotic genes. In terms of phylogeny, the 100 most vertically evolving prokaryotic genes are neither representative nor predictive for the remaining 97% of an average genome. In search of factors that govern LGT frequency, we find a simple but natural principle: Verticality correlates strongly with gene distribution density, LGT being least likely for intruding genes that must replace a preexisting homologue in recipient chromosomes. LGT is most likely for novel genetic material, intruding genes that encounter no competing copy.

The last eukaryote common ancestor (LECA) possessed mitochondria and all key traits that make eukaryotic cells more complex than their prokaryotic ancestors, yet the timing of mitochondrial acquisition and the role of mitochondria in the origin of eukaryote complexity remain debated. Here we report evidence from gene duplications in LECA indicating an early origin of mitochondria. Among 163,545 duplications in 24,571 gene trees spanning 150 sequenced eukaryotic genomes, we identify 713 gene duplication events that occurred in LECA. LECA's bacterial derived genes include numerous mitochondrial functions and were duplicated significantly more often than archaeal derived and eukaryote specific genes. The surplus of bacterial derived duplications in LECA most likely reflects the serial copying of genes from the mitochondrial endosymbiont to the archaeal host's chromosomes. Clustering, phylogenies and likelihood ratio tests for 22.4 million genes from 5,655 prokaryotic and 150 eukaryotic genomes reveal no evidence for lineage specific gene acquisitions in eukaryotes, except from the plastid in the plant lineage. That finding, and the functions of bacterial genes duplicated in LECA, suggest that the bacterial genes in eukaryotes are acquisitions from the mitochondrion, followed by vertical gene evolution and differential loss across eukaryotic lineages, flanked by concomitant lateral gene transfer among prokaryotes. Overall, the data indicate that recurrent gene transfer via the copying of genes from a resident mitochondrial endosymbiont to archaeal host chromosomes preceded the onset of eukaryotic cellular complexity, favoring mitochondria-early over mitochondria-late hypotheses for eukaryote origin.

The question concerning the meaning of life is important, but it immediately confronts the present authors with insurmountable obstacles from a philosophical standpoint, as it would require us to define not only what we hold to be life, but what we hold to be meaning in addition, requiring us to do both in a properly researched context. We unconditionally surrender to that challenge. Instead, we offer a vernacular, armchair approach to life’s origin and meaning, with some layman’s thoughts on the meaning of origins as viewed from the biologist’s standpoint. One can observe that biologists generally approach the concept of biological meaning in the context of evolution. This is the basis for the broad resonance behind Dobzhansky’s appraisal that “Nothing in biology makes sense except in the light of evolution”. Biologists try to understand living things in the historical context of how they arose, without giving much thought to the definition of what life or living things are, which for a biologist is usually not an interesting question in the practical context of daily dealings with organisms. Do humans generally understand life’s meaning in the context of history? If we consider the problem of life’s origin, the question of what constitutes a living thing becomes somewhat more acute for the biologist, though not more answerable, because it is inescapable that there was a time when there were no organisms on Earth, followed by a time when there were, the latter time having persisted in continuity to the present. This raises the question of where, in that transition, chemicals on Earth became alive, requiring, in turn, a set of premises for how life arose in order to conceptualize the problem in relation to organisms we know today, including ourselves, which brings us to the point of this paper: In the same way that cultural narratives for origins always start with a setting, scientific narratives for origins also always start with a setting, a place on Earth or elsewhere where we can imagine what happened for the sake of structuring both the problem and the narrative for its solution. This raises the question of whether scientific origins settings convey meaning to humans in that they suggest to us from what kind of place and what kinds of chemicals we are descended, that is, to which inanimate things we are most closely related.