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.

Highlights

  • Natural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms

  • Expressed gene contigs encompassing the carbohydrate-binding module (CBM) present at the C terminus of cellulases, were identified in all seven Pristionchus species and a near full-length cellulase transcript was found in Koerneria sudhausi (Figure 1A) [18]

  • The CBM of the Pristionchus nematodes belonged to the CBM49 family [19] and differed from that of plant-parasitic nematodes, which have similarity to the bacterial carbohydratebinding module of family 2 (CBM2; pfam00553) [18]

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Summary

Introduction

Natural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms. Recent genome and expressed sequence tag (EST) projects in nematodes provide strong evidence for HGT from bacteria, fungi, amoebozoa or from endosymbionts in the plant parasites Meloidogyne incognita and M. hapla, fungivorous and Surprisingly, phylogenetic reconstruction suggests that cellulase genes have been acquired multiple times independently in nematodes from distinct microbial donors [9]. Characterized cellulases from plant parasitic Tylenchida (plant sedentary endoparasitic nematodes such as Meloidogyne, Heterodera and Globodera) and migratory parasitic species (Pratylenchus penetrans) are from glycoside hydrolase family 5 (GHF5). They appear to have acquired a whole ancestral GHF5 gene cassette consisting of the catalytic domain and the carbohydratebinding module 2 (CBM2) [10]. Genes obtained by HGT that are central to parasitic interaction, like pectin lyase or cellulase genes have undergone expansion by gene duplication after HGT in Meloidogyne hapla, M. incognita or P. pacificus [5,6,7,10]

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