Role of horizontal gene transfer in the evolution of plant parasitism among nematodes.

Horizontal gene transfer (HGT) implies the non-sexual exchange of genetic material between species - in some cases even across kingdoms. Although common among Bacteria and Archaea, HGTs from pro- to eukaryotes and between eukaryotes were thought to be extremely rare. Recent studies on intracellular bacteria and their hosts seriously question this view. Recipient organisms could benefit from HGT as new gene packages could allow them to broaden or change their diet, colonize new habitats, or survive conditions that previously would have been lethal.About a decade ago, plant parasitic nematodes were shown to produce and secrete cellulases. Prior to this, animals were thought to fully depend on microbial symbionts for the breakdown of plant cell walls. This discovery prompted Keen and Roberts (1) to hypothesize that the ability of nematodes to parasitize plants was acquired by HGT from soil bacteria to (ancestral) bacterivorous nematodes. Since the identification of the first nematode cellulases, many more plant cell wall-degrading enzymes (CWDE) have been identified in a range of plant parasitic nematode species.Here we discuss a number of criteria that can be used to underpin an HGT claim. HGT requires close physical contact between donor and recipient, and this could be achieved in, for example, a symbiont-host, or a trophic relationship. The former type of relationship was indeed shown to potentially result in the transfer of genetic material (e.g., Brugia malayi and Wolbachia). However, currently known endosymbionts of nematodes may not be the source of CWDEs. Remarkably, all cellulases discovered so far within the order Tylenchida belong to a single glycoside hydrolase family (GHF5). A range of soil bacteria harbours GHF5 cellulases, but of course nothing can be said about the gene content of soil bacteria at the time HGT took place (if at all). We suggest that characterisation of cellulases (and other CWDEs) and their genomic organisation in more basal (facultative) plant parasitic Tylenchida is needed to find out if CWDEs were indeed acquired via HGT from bacteria. A more complete picture about the evolution of CWDEs among plant parasitic Tylenchida will require a detailed characterisation of two - so far - fully unexplored basal suborders, Tylenchina and Criconematina. Finally, we performed a computational high-throughput identification of potential HGT candidates (including ones unrelated to CWDEs) in plant parasitic nematodes using a genomics approach.