Abstract
BackgroundPlant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls. Among the cell wall-degrading enzymes, glycoside hydrolase family 5 (GHF5) cellulases are relatively well characterized, especially for high impact parasites such as root-knot and cyst nematodes. Interestingly, ancestors of extant nematodes most likely acquired these GHF5 cellulases from a prokaryote donor by one or multiple lateral gene transfer events. To obtain insight into the origin of GHF5 cellulases among evolutionary advanced members of the order Tylenchida, cellulase biodiversity data from less distal family members were collected and analyzed.ResultsSingle nematodes were used to obtain (partial) genomic sequences of cellulases from representatives of the genera Meloidogyne, Pratylenchus, Hirschmanniella and Globodera. Combined Bayesian analysis of ≈ 100 cellulase sequences revealed three types of catalytic domains (A, B, and C). Represented by 84 sequences, type B is numerically dominant, and the overall topology of the catalytic domain type shows remarkable resemblance with trees based on neutral (= pathogenicity-unrelated) small subunit ribosomal DNA sequences. Bayesian analysis further suggested a sister relationship between the lesion nematode Pratylenchus thornei and all type B cellulases from root-knot nematodes. Yet, the relationship between the three catalytic domain types remained unclear. Superposition of intron data onto the cellulase tree suggests that types B and C are related, and together distinct from type A that is characterized by two unique introns.ConclusionsAll Tylenchida members investigated here harbored one or multiple GHF5 cellulases. Three types of catalytic domains are distinguished, and the presence of at least two types is relatively common among plant parasitic Tylenchida. Analysis of coding sequences of cellulases suggests that root-knot and cyst nematodes did not acquire this gene directly by lateral genes transfer. More likely, these genes were passed on by ancestors of a family nowadays known as the Pratylenchidae.
Highlights
Plant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls
In all of the nematodes we identified at least one glycoside hydrolase family 5 (GHF5) cellulase gene (Table 2)
The latter two substrates were not significantly degraded by Hg-ENG-1 and −4 [28]. As such differences have been reported for other GHF5 cellulases as well (e.g. [29]), we hypothesize that the different types of catalytic domains could point at differences in substrate specificities
Summary
Plant parasitic nematodes are unusual Metazoans as they are equipped with genes that allow for symbiont-independent degradation of plant cell walls. Ancestors of extant nematodes most likely acquired these GHF5 cellulases from a prokaryote donor by one or multiple lateral gene transfer events. The transfer of a gene related to malaria sporozoite invasion from mosquito to its endosymbiotic bacterium Wolbachia pipientis was demonstrated by Woolfit et al (2008, [1]). This gene showed substantial divergence, and the level of expression suggested it to be functional in the new prokaryote host. The pea aphid Acyrthisiphon pisum probably acquired two genes from bacteria by LGT [2] These laterally transferred genes are expressed in the bacteriocytes, and they contribute to the maintenance of Buchnera aphidicola, the aphid’s primary symbiont. The authors hypothesized that LGT could be facilitated by mechanisms underlying the desiccation tolerance of this rotifer
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