The Extent of Genome Flux and Its Role in the Differentiation of Bacterial Lineages

Abstract

Horizontal gene transfer (HGT) and gene loss are key processes in bacterial evolution. However, the role of gene gain and loss in the emergence and maintenance of ecologically differentiated bacterial populations remains an open question. Here, we use whole-genome sequence data to quantify gene gain and loss for 27 lineages of the plant-associated bacterium Pseudomonas syringae. We apply an extensive error-control procedure that accounts for errors in draft genome data and greatly improves the accuracy of patterns of gene occurrence among these genomes. We demonstrate a history of extensive genome fluctuation for this species and show that individual lineages could have acquired thousands of genes in the same period in which a 1% amino acid divergence accrues in the core genome. Elucidating the dynamics of genome fluctuation reveals the rapid turnover of gained genes, such that the majority of recently gained genes are quickly lost. Despite high observed rates of fluctuation, a phylogeny inferred from patterns of gene occurrence is similar to a phylogeny based on amino acid replacements within the core genome. Furthermore, the core genome phylogeny suggests that P. syringae should be considered a number of distinct species, with levels of divergence at least equivalent to those between recognized bacterial species. Gained genes are transferred from a variety of sources, reflecting the depth and diversity of the potential gene pool available via HGT. Overall, our results provide further insights into the evolutionary dynamics of genome fluctuation and implicate HGT as a major factor contributing to the diversification of P. syringae lineages.

Rates of Lateral Gene Transfer in Prokaryotes: High but Why?

“…In most studies this is apparent from a decrease in the rate of gene content change relative to the rate of nucleotide substitution in the deeper branches of the phylogeny compared to the tips. The same pattern is most elegantly demonstrated in the P. syringae and E. coli studies [21,22] in which the vast majority of individual gene gains are mapped to a single strain. There are three potential explanations for why most gene content changes are transient.…”

“…Similar estimates were found in Streptococcus [19] and Corynebacterium [20] genomes using the same methodology. A recent estimate of LGT rate in Pseudomonas syringae based on stochastic mapping methodology (after corrections necessary for working with genomes that are not sequenced to complete closure) was found to be four orders of magnitude higher than the estimate for B. cereus [21]. Individual P. syringae lineages could be shown to have acquired thousands of genes in the same period in which a 1% amino acid divergence accrued in the core genome.…”

How and Why to Build a Unified Tree of Life

“…[49] In addition, genes that are gained seem to be labile through evolutionary time, and are readily lost, while mutations tracing vertical phylogenetic signal continue to accumulate in the core genome. [50] Recent analyses of HGT across genomes suggest that long term successful transfer of genes across lineages is rare, [49] leaving phylogenetic structure intact. [51] These results are consistent with the observation that bacteria do form biologically coherent groups, which would not be expected if horizontal gene flow were rampant and unconstrained.…”

Adaptation in Natural Microbial Populations

“…Likewise, it has been shown that new gene copies arise more often through LGT than through duplication (Treangen & Rocha 2011), and population genomic studies have revealed that isolates with nearly 5 identical nucleotide composition in the genes they share can differ by many hundreds of accessory genes (e.g. (Nowell et al 2014)), indicating that LGT might be more important than mutation. Indeed, over large evolutionary timescales LGT events can completely transform the genomic make-up, metabolism and ecological life-styles of bacterial lineages (e.g.…”