A spectrum of verticality across genes

Abstract

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 metabolic network of the last bacterial common ancestor

“…But is the ubiquitous nature of these genes caused by their antiquity, or is it the result of LGT? To address this question, we obtained all values of verticality for prokaryotic gene families 29 as a proxy to measure the gene’s tendency to undergo or resist LGT. LBCA’s protein families are distinctively and significantly (Kolgomorov–Smirnov statistic = 0.99, p value = 2.4e – 318) more vertical than the average prokaryotic protein family (Fig.…”

“…All 261,058 values of verticality for all prokaryotic gene families were obtained from Nagies et al 29 , where the highest possible value is 24 and the lowest is zero. All LBCA protein families were ranked from most to least vertical (Supplementary Data 7 ).…”

“…Metabolic networks include multiple redundant paths, and in different species, different routes can lead to the same functional outcome. Because metabolism is far more variable across lineages than the information processing machinery, the genes coding for enzymes are not universal across genomes and are much more prone to undergo LGT than information processing genes are 29 . This circumstance has impaired the use of metabolic enzymes for the study of early prokaryotic evolution.…”

Host Range and Coding Potential of Eukaryotic Giant Viruses

“…Even more challenging is to understand and predict genome variation across giant viruses. Rampant occurrence of LGTs is known to cause extensive gene content variation in prokaryotes, even among strains with highly similar core gene sequences [ 149 , 150 , 151 ], such that the 3% most vertically inherited genes are not predictive of the rest of the genome [ 152 ]. With limited evidence for long-term verticality plus substantial genome size differences, little can be inferred about giant virus gene contents from a phylogenetic tree based on a concatenated alignment of 10 genes that are not devoid of conflicting signals.…”

Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction

“…In gradualist theories, the host is assumed to be a descendant of the archaeal lineage, one that had however passed the threshold from prokaryotic to eukaryotic cell complexity by evolutionary mechanisms other than symbiosis, thereby bridging the gap between prokaryotic and eukaryotic complexity ( Martijn and Ettema 2013 ; Spang et al 2015 ) before the origin of mitochondria, which therefore had little impact on eukaryote complexity. In hybrid theories, the prokaryote to eukaryote transition involved one or more additional symbioses that preceded the origin of mitochondria, such as flagella (Sagan 1967), peroxisomes ( de Duve 1969 ), the nucleus ( López-García and Moreira 2020 ), or the ER ( Gupta and Golding, 1996 ), or was precipitated by lateral gene transfer (LGT) to the host lineage, such that many hallmark traits of eukaryotes stem from genes that were invented in foreign lineages and donated to LECA via LGT ( Pittis and Gabaldón 2016 ; Vosseberg et al 2021 ) although the methods underpinning such claims have been called into question ( Martin et al, 2017a ; Tria et al 2019 ; Nagies et al, 2020 ). Gradualist and hybrid theories typically posit an origin of phagotrophic feeding within the archaeal host lineage before the origin of mitochondria ( Doolittle, 1998 ; Spang et al, 2015 ; Zaremba-Niedzwiedzka et al, 2017 ; Vosseberg et al 2021 ), which is however a deeply problematic proposition from the physiological standpoint ( Martin et al 2017b ) and at odds with evidence from the microfossil record indicating a late origin of phagocytosis ( Mills, 2020 ).…”