Lateral gene transfer is an important mechanism of natural variation among prokaryotes, but the significance of its quantitative contribution to genome evolution is debated. Here, we report networks that capture both vertical and lateral components of evolutionary history among 539,723 genes distributed across 181 sequenced prokaryotic genomes. Partitioning of these networks by an eigenspectrum analysis identifies community structure in prokaryotic gene-sharing networks, the modules of which do not correspond to a strictly hierarchical prokaryotic classification. Our results indicate that, on average, at least 81 ± 15% of the genes in each genome studied were involved in lateral gene transfer at some point in their history, even though they can be vertically inherited after acquisition, uncovering a substantial cumulative effect of lateral gene transfer on longer evolutionary time scales.

As lateral gene transfer among prokaryotes and endosymbiotic gene transfer (from organelles) among eukaryotes are fundamentally not tree-like in nature, biologists need to depart from the notion that all genomes are related by a single bifurcating tree.

Plasmid acquisition is an important mechanism of rapid adaptation and niche expansion in prokaryotes. Positive selection for plasmid-coded functions is a major driver of plasmid evolution, while plasmids that do not confer a selective advantage are considered costly and expected to go extinct. Yet, plasmids are ubiquitous in nature, and their persistence remains an evolutionary paradox. Here, we demonstrate that non-mobile plasmids persist over evolutionary timescales without selection for the plasmid function. Evolving a minimal plasmid encoding for antibiotics resistance in Escherichia coli, we discover that plasmid stability emerges in the absence of antibiotics and that plasmid loss is determined by transcription-replication conflicts. We further find that environmental conditions modulate these conflicts and plasmid persistence. Silencing the transcription of the resistance gene results in stable plasmids that become fixed in the population. Evolution of plasmid stability under non-selective conditions provides an evolutionary explanation for the ubiquity of plasmids in nature.

Lateral gene transfer (LGT) plays a major role in prokaryote evolution with only a few genes that are resistant to it; yet the nature and magnitude of barriers to lateral transfer are still debated. Here, we implement directed networks to investigate donor–recipient events of recent lateral gene transfer among 657 sequenced prokaryote genomes. For 2,129,548 genes investigated, we detected 446,854 recent lateral gene transfer events through nucleotide pattern analysis. Among these, donor–recipient relationships could be specified through phylogenetic reconstruction for 7% of the pairs, yielding 32,028 polarized recent gene acquisition events, which constitute the edges of our directed networks. We find that the frequency of recent LGT is linearly correlated both with genome sequence similarity and with proteome similarity of donor–recipient pairs. Genome sequence similarity accounts for 25% of the variation in gene-transfer frequency, with proteome similarity adding only 1% to the variability explained. The range of donor–recipient GC content similarity within the network is extremely narrow, with 86% of the LGTs occurring between donor–recipient pairs having ≤5% difference in GC content. Hence, genome sequence similarity and GC content similarity are strong barriers to LGT in prokaryotes. But they are not insurmountable, as we detected 1530 recent transfers between distantly related genomes. The directed network revealed that recipient genomes of distant transfers encode proteins of nonhomologous end-joining (NHEJ; a DNA repair mechanism) far more frequently than the recipient lacking that mechanism. This implicates NHEJ in genes spread across distantly related prokaryotes through bypassing the donor–recipient sequence similarity barrier.

Cyanobacteria forged two major evolutionary transitions with the invention of oxygenic photosynthesis and the bestowal of photosynthetic lifestyle upon eukaryotes through endosymbiosis. Information germane to understanding those transitions is imprinted in cyanobacterial genomes, but deciphering it is complicated by lateral gene transfer (LGT). Here, we report genome sequences for the morphologically most complex true-branching cyanobacteria, and for Scytonema hofmanni PCC 7110, which with 12,356 proteins is the most gene-rich prokaryote currently known. We investigated components of cyanobacterial evolution that have been vertically inherited, horizontally transferred, and donated to eukaryotes at plastid origin. The vertical component indicates a freshwater origin for water-splitting photosynthesis. Networks of the horizontal component reveal that 60% of cyanobacterial gene families have been affected by LGT. Plant nuclear genes acquired from cyanobacteria define a lower bound frequency of 611 multigene families that, in turn, specify diazotrophic cyanobacterial lineages as having a gene collection most similar to that possessed by the plastid ancestor.