Abstract
Single copy genes, universally distributed across the three domains of life and encoding mostly ancient parts of the translation machinery, are thought to be only rarely subjected to horizontal gene transfer (HGT). Indeed it has been proposed to have occurred in only a few genes and implies a rare, probably not advantageous event in which an ortholog displaces the original gene and has to function in a foreign context (orthologous gene displacement, OGD). Here, we have utilised an automatic method to identify HGT based on a conservative statistical approach capable of robustly assigning both donors and acceptors. Applied to 40 universally single copy genes we found that as many as 68 HGTs (implying OGDs) have occurred in these genes with a rate of 1.7 per family since the last universal common ancestor (LUCA). We examined a number of factors that have been claimed to be fundamental to HGT in general and tested their validity in the subset of universally distributed single copy genes. We found that differing functional constraints impact rates of OGD and the more evolutionarily distant the donor and acceptor, the less likely an OGD is to occur. Furthermore, species with larger genomes are more likely to be subjected to OGD. Most importantly, regardless of the trends above, the number of OGDs increases linearly with time, indicating a neutral, constant rate. This suggests that levels of HGT above this rate may be indicative of positively selected transfers that may allow niche adaptation or bestow other benefits to the recipient organism.
Highlights
From the earliest comparative genomic studies it was obvious that horizontal gene transfer (HGT) occurred frequently [1,2,3] and would impinge upon our efforts to understand the evolutionary history of all life [4,5,6,7,8]
This tree was used in an exhaustive maximum likelihood procedure where the sequence data for each individual gene family was used to determine the best phylogenetic placement of every branch of the tree, identifying when this indicated a possible orthologous gene displacement (Figure 1)
By developing a new method for the identification and positionspecific masking of OGDs, we could quantify the large number of events that have occurred in 40 gene families that have been in existence since the last universal common ancestor
Summary
From the earliest comparative genomic studies it was obvious that horizontal gene transfer (HGT) occurred frequently [1,2,3] and would impinge upon our efforts to understand the evolutionary history of all life [4,5,6,7,8]. We focussed on the approximately 1% [25] of gene families that are universally single copy [14], and likely have been functionally preserved since the emergence of the three domains of life When these genes are successfully subjected to HGT, they should maintain the interactions of the original copy that they displace (orthologous gene displacement (OGD) [26]). It has been suggested that even marginal differences in sequence identity between the displaced copy and it’s replacement is enough to cause a marked decrease in fitness of the acceptor organism [27], requiring compensatory evolutionary change to occur This suggests that the successful fixation of an OGD in these genes requires overcoming the most stringent barriers of any horizontal transfer event [20]. These characteristics make HGTs in these genes potentially important for the elucidation of constraints and promoting factors of HGT in general
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