Distribution and evolution of glycoside hydrolase family 45 cellulases in nematodes and fungi.

Juan E Palomares-Rius,Hayato Masuya,John T Jones,Isheng J Tsai,Akina Hino,Natsumi Kanzaki,Yuuri Hirooka,Taisei Kikuchi

doi:10.1186/1471-2148-14-69

Abstract

BackgroundHorizontal gene transfer (HGT) has been suggested as the mechanism by which various plant parasitic nematode species have obtained genes important in parasitism. In particular, cellulase genes have been acquired by plant parasitic nematodes that allow them to digest plant cell walls. Unlike the typical glycoside hydrolase (GH) family 5 cellulase genes which are found in several nematode species from the order Tylenchida, members of the GH45 cellulase have only been identified in a cluster including the families Parasitaphelenchidae (with the pinewood nematode Bursaphelenchus xylophilus) and Aphelenchoididae, and their origins remain unknown.ResultsIn order to investigate the distribution and evolution of GH45 cellulase genes in nematodes and fungi we performed a wide ranging screen for novel putative GH45 sequences. This revealed that the sequences are widespread mainly in Ascomycetous fungi and have so far been found in a single major nematode lineage. Close relationships between the sequences from nematodes and fungi were found through our phylogenetic analyses. An intron position is shared by sequences from Bursaphelenchus nematodes and several Ascomycetous fungal species.ConclusionsThe close phylogenetic relationships and conserved gene structure between the sequences from nematodes and fungi strongly supports the hypothesis that nematode GH45 cellulase genes were acquired via HGT from fungi. The rapid duplication and turnover of these genes within Bursaphelenchus genomes demonstrate that useful sequences acquired via HGT can become established in the genomes of recipient organisms and may open novel niches for these organisms to exploit.

Highlights

Horizontal gene transfer (HGT) has been suggested as the mechanism by which various plant parasitic nematode species have obtained genes important in parasitism
Amplification of GH45 cellulase sequences Genomic DNA was extracted from 289 fungal species/ strains and 26 nematode species/strains (Additional file 1: Table S1, S2) and used for PCR amplification with a degenerate primer pair designed from a conserved region of known GH45 cellulases (Additional file 2: Figure S1)
For fungi 70 GH45-like sequences were identified from 61 fungal species, all of which belong to Ascomycota (Additional file 1: Table S4)

Summary

Introduction

Horizontal gene transfer (HGT) has been suggested as the mechanism by which various plant parasitic nematode species have obtained genes important in parasitism. Cellulase genes have been acquired by plant parasitic nematodes that allow them to digest plant cell walls. Unlike the typical glycoside hydrolase (GH) family 5 cellulase genes which are found in several nematode species from the order Tylenchida, members of the GH45 cellulase have only been identified in a cluster including the families Parasitaphelenchidae (with the pinewood nematode Bursaphelenchus xylophilus) and Aphelenchoididae, and their origins remain unknown. Many microorganisms produce cellulases to degrade cellulose in order to use it as a carbon source. Recent studies have shown that some insects and plant-parasitic nematodes have endogenous cellulases that degrade cellulose polymers [1,2]. Fourteen families of glycosyl hydrolases (GH) are known to include proteins that degrade cellulose (http://www.cazy.org). It is thought that proteins within each group are structurally related and are likely to have evolved from a common ancestor [4]

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Conclusion