The fate of laterally transferred genes: Life in the fast lane to adaptation or death

Abstract

Large-scale genome arrangement plays an important role in bacterial genome evolution. A substantial number of genes can be inserted into, deleted from, or rearranged within genomes during evolution. Detecting or inferring gene insertions/deletions is of interest because such information provides insights into bacterial genome evolution and speciation. However, efficient inference of genome events is difficult because genome comparisons alone do not generally supply enough information to distinguish insertions, deletions, and other rearrangements. In this study, homologous genes from the complete genomes of 13 closely related bacteria were examined. The presence or absence of genes from each genome was cataloged, and a maximum likelihood method was used to infer insertion/deletion rates according to the phylogenetic history of the taxa. It was found that whole gene insertions/deletions in genomes occur at rates comparable to or greater than the rate of nucleotide substitution and that higher insertion/deletion rates are often inferred to be present at the tips of the phylogeny with lower rates on more ancient interior branches. Recently transferred genes are under faster and relaxed evolution compared with more ancient genes. Together, this implies that many of the lineage-specific insertions are lost quickly during evolution and that perhaps a few of the genes inserted by lateral transfer are niche specific.

Does Gene Translocation Accelerate the Evolution of Laterally Transferred Genes?

“…Conserved specific genes have greater K a /K s values than conserved nonspecific genes in all genome pairs. This is consistent with previous findings that recently transferred genes have faster rates of evolution (Hao and Golding 2006b). In nonspecific genes, translocated genes have faster rates of evolution over positionally conserved genes in the BlBp, BamBs, and BwBc 4 genome pairs, suggesting that translocated genes tend to have greater rates of evolution over positionally conserved genes.…”

“…This trend is the opposite of the result that ancient genes have a higher proportion of genes on the leading strand than overall group specific genes (Figure 7). The result of more recently acquired genes on the leading strand could not be explained by the essentiality of recently acquired genes, since previous analyses have shown faster evolutionary rates and higher K a /K s ratios in more recently acquired genes (Hao and Golding 2006b). Genes and the ISs and prophage regions in the Ba 1 genome were mapped on the chromosome (see Figure S3).…”

Estimation of Gene Insertion/Deletion Rates with Missing Data

“…The transition rate matrix representing the probabilities of a transition from one state to the next can be easily derived (cf. Hao and Golding 2006),…”

“…This reflects the sampling bias. A correction for the sampling bias (Felsenstein 1992;Lewis 2001;Hao and Golding 2006;Cohen and Pupko 2010) can be imposed such that the probability is conditional on observing the gene in at least one species,…”

A likelihood framework to analyse phyletic patterns

“…Initial approaches towards this goal were based on the Dollo parsimony criterion (Mirkin et al 2003). More advanced models were based on the maximum-likelihood (ML) paradigm (Hao & Golding 2006); however, they assumed that the gain rate is equal to the loss rate, thus ensuring that the genome sizes do not change. Nevertheless, as stated by these authors, this assumption is unlikely to be correct, given evidence that even within closely related species genome content may change considerably (Thompson et al 2005).…”