Contribution of Lateral Gene Transfers to the Genome Composition and Parasitic Ability of Root-Knot Nematodes

Abstract

Lateral gene transfers (LGT), species to species transmission of genes by means other than direct inheritance from a common ancestor, have played significant role in shaping prokaryotic genomes and are involved in gain or transfer of important biological processes. Whether LGT significantly contributed to the composition of an animal genome is currently unclear. In nematodes, multiple LGT are suspected to have favored emergence of plant-parasitism. With the availability of whole genome sequences it is now possible to assess whether LGT have significantly contributed to the composition of an animal genome and to establish a comprehensive list of these events. We generated clusters of homologous genes and automated phylogenetic inference, to detect LGT in the genomes of root-knot nematodes and found that up to 3.34% of the genes originate from LGT of non-metazoan origin. After their acquisition, the majority of genes underwent series of duplications. Compared to the rest of the genes in these species, several predicted functional categories showed a skewed distribution in the set of genes acquired via LGT. Interestingly, functions related to metabolism, degradation or modification of carbohydrates or proteins were substantially more frequent. This suggests that genes involved in these processes, related to a parasitic lifestyle, have been more frequently fixed in these parasites after their acquisition. Genes from soil bacteria, including plant-pathogens were the most frequent closest relatives, suggesting donors were preferentially bacteria from the rhizosphere. Several of these bacterial genes are plasmid-borne, pointing to a possible role of these mobile genetic elements in the transfer mechanism. Our analysis provides the first comprehensive description of the ensemble of genes of non-metazoan origin in an animal genome. Besides being involved in important processes regarding plant-parasitism, genes acquired via LGT now constitute a substantial proportion of protein-coding genes in these nematode genomes.

Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life

“…Some of these proteins could originate from HGT events. To assess which AI threshold maximizes the number of very likely HGT and minimizes the number of false positives, we compared the results of Alienness to a previous analysis we published on the same proteome in 2012 [38]. Briefly, in this 2012 analysis we first identified Meloidogyne proteins having no clear ortholog in metazoa via an OrthoMCL analysis [39].…”

“…To estimate the recall rate of Alienness, we plotted the percentage of candidate HGT proteins supported by phylogenies ( Figure 5) for different AI threshold values (from -10 to >66 with incremental steps of 2). We differentiate phylogenies only supported by a node 'A' linking the plant-parasitic nematodes to non-metazoan putative donors and those supported by both a node 'A' and an additional node 'B', linking the node 'A' to any species but plant-parasitic nematodes [38]. To estimate the risk of false positives produced by Alienness, we plotted the percentage of proteins returning phylogenetic trees not supporting HGT at the same range of AI values.…”

Horizontal gene transfer in the sponge Amphimedon queenslandica

“…The sequences from all known proteins from bacterial plasmids, prophages and phages were downloaded from the ACLAME database (version 4.0; http://aclame.ulb.ac.be/perl/Aclame/Tools/exporter.cgi; Leplae et al 2010) and formatted as a custom database in Geneious Pro 5.1.7 (www.geneious.com; Kearse et al 2012). The Aqu2.1 gene models of the 576 AqHGT-derivatives were searched against this custom database using BLASTp in Geneious Pro 5.1.7 (www.geneious.com; Kearse et al 2012), with the same cut-off thresholds used by Paganini et al (2012) in their similar search (e-value <0.001, with at least 30% identity on at least 50% of both the query and subject proteins).…”

“…While there are many speculations about TEs mediating HGT in animals, only two studies have systematically tested for a genomic co-occurrence of HGTs and TEs in animals, as summarised above (Paganini et al 2012;Flot et al 2013). However, neither of these studies considered the possibly confounding effect of gene duplication on their analysis, despite reporting extensive duplications of HGTs (Paganini et al 2012;Flot et al 2013).…”

“…However, neither of these studies considered the possibly confounding effect of gene duplication on their analysis, despite reporting extensive duplications of HGTs (Paganini et al 2012;Flot et al 2013). Here, I investigate and compare the densities and content of bacterial and eukaryotic TEs around putatively unduplicated HGTs and native genes in the genome of A. queenslandica.…”