Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover

Abstract

BackgroundNatural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms. There is now growing evidence that horizontal gene transfer also plays important roles in the evolution of eukaryotes. Genome-sequencing and EST projects of plant and animal associated nematodes such as Brugia, Meloidogyne, Bursaphelenchus and Pristionchus indicate horizontal gene transfer as a key adaptation towards parasitism and pathogenicity. However, little is known about the functional activity and evolutionary longevity of genes acquired by horizontal gene transfer and the mechanisms favoring such processes.ResultsWe examine the transfer of cellulase genes to the free-living and beetle-associated nematode Pristionchus pacificus, for which detailed phylogenetic knowledge is available, to address predictions by evolutionary theory for successful gene transfer. We used transcriptomics in seven Pristionchus species and three other related diplogastrid nematodes with a well-defined phylogenetic framework to study the evolution of ancestral cellulase genes acquired by horizontal gene transfer. We performed intra-species, inter-species and inter-genic analysis by comparing the transcriptomes of these ten species and tested for cellulase activity in each species. Species with cellulase genes in their transcriptome always exhibited cellulase activity indicating functional integration into the host's genome and biology. The phylogenetic profile of cellulase genes was congruent with the species phylogeny demonstrating gene longevity. Cellulase genes show notable turnover with elevated birth and death rates. Comparison by sequencing of three selected cellulase genes in 24 natural isolates of Pristionchus pacificus suggests these high evolutionary dynamics to be associated with copy number variations and positive selection.ConclusionWe could demonstrate functional integration of acquired cellulase genes into the nematode's biology as predicted by theory. Thus, functional assimilation, remarkable gene turnover and selection might represent key features of horizontal gene transfer events in nematodes.

Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

“…Compared to the reference genome, 7.2% (median, IQR: 6.8-7.4%) and 2.4% (median, IQR: 2.3-2.6%) of the genome were predicted as deleted and duplicated, respectively. We verified predicted deletions with PCR amplification experiments for three cellulase genes in 24 strains and found perfect agreement (Mayer et al 2011). Genome-wide levels of nucleotide diversity Figure 1B shows the phylogenetic relationship of the 104 sequenced strains as a split network.…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…Analyses of the complete genome of the necromenic nematode Pristionchus pacificus and transcriptomic studies reveal that several functional cellulase genes have been transferred to the ancestor of the Pristionchus genus from bacterial donors [27][28][29]. These cellulase genes are unrelated to the cellulase genes found in plant-parasitic nematodes (see below).…”

Evolution of Bacterial-Like Phosphoprotein Phosphatases in Photosynthetic Eukaryotes Features Ancestral Mitochondrial or Archaeal Origin and Possible Lateral Gene Transfer

“…Over time, however, it has become apparent that alternative modes of eukaryotic gene and protein acquisition exist, such as independent horizontal or lateral gene transfer (LGT) events (Keeling and Palmer, 2008;Keeling, 2009). Targeted studies of protein evolution have seen a steady rise in documented LGT events across a wide variety of eukaryotic organisms, including photosynthetic eukaryotes (Derelle et al, 2006;Raymond and Kim, 2012;Schönknecht et al, 2013), nematodes (Mayer et al, 2011), arthropods (Acuña et al, 2012), fungi (Wenzl et al, 2005), amoebozoa (Clarke et al, 2013), and oomycetes (Belbahri et al, 2008). Each instance documents the integration of a bacterial gene(s) into a eukaryotic organism, seemingly resulting in an adaptive advantage(s) important to organism survival.…”