Transposases are the most abundant, most ubiquitous genes in nature

Abstract

Genes, like organisms, struggle for existence, and the most successful genes persist and widely disseminate in nature. The unbiased determination of the most successful genes requires access to sequence data from a wide range of phylogenetic taxa and ecosystems, which has finally become achievable thanks to the deluge of genomic and metagenomic sequences. Here, we analyzed 10 million protein-encoding genes and gene tags in sequenced bacterial, archaeal, eukaryotic and viral genomes and metagenomes, and our analysis demonstrates that genes encoding transposases are the most prevalent genes in nature. The finding that these genes, classically considered as selfish genes, outnumber essential or housekeeping genes suggests that they offer selective advantage to the genomes and ecosystems they inhabit, a hypothesis in agreement with an emerging body of literature. Their mobile nature not only promotes dissemination of transposable elements within and between genomes but also leads to mutations and rearrangements that can accelerate biological diversification and--consequently--evolution. By securing their own replication and dissemination, transposases guarantee to thrive so long as nucleic acid-based life forms exist.

Figure 1.

Abundance of different functional roles in 2137 genomes plotted against the ubiquity of these functional roles (defined as the number of genomes in which the functional role is represented at least once). r, Pearson’s product moment correlation between abundance and ubiquity; Cys, cysteine; Thio, thioredoxin; ThioR, thioredoxin reductase. Proteins annotated solely based on their location or posttranslational modification but not their biological functions (e.g. membrane proteins, cytoplasmic proteins, secreted proteins, transmembrane proteins and generic lipoproteins) were excluded; an exception was the ‘outer membrane protein’ annotation as it describes specific bacterial proteins rather than protein localization.

Figure 2.

The normalized cumulative abundance indices (nCAI) of different functional roles in 187 metagenomes plotted against the ubiquity of these functional roles (defined as the number of metagenomes in which the functional role is represented at least once). r, Pearson’s product moment correlation between abundance and ubiquity; DNA Pol, DNA polymerase; dTDP-G 4,6 DH, dTDP-glucose 4,6 dehydratase; Rep, replication-associated protein; RNR, ribonuleotide reductase; SSB, single-stranded DNA-binding protein; ThyX, thymidylate synthase thyX (EC 2.1.1.-); UDP-G 4-epi, UDP-glucose 4-epimerase.

Figure 3.

Word clouds (created on http://www.wordle.net) representing (A) the 100 most abundant functional roles (Supplementary Table S3) and (B) the 100 most ubiquitous functional roles (Supplementary Table S4) in metagenomes. The font size of each functional role is proportional to its (A) abundance index or (B) number of metagenomes in which it is present.

Figure 3.

Word clouds (created on http://www.wordle.net) representing (A) the 100 most abundant functional roles (Supplementary Table S3) and (B) the 100 most ubiquitous functional roles (Supplementary Table S4) in metagenomes. The font size of each functional role is proportional to its (A) abundance index or (B) number of metagenomes in which it is present.