Abstract
BackgroundHoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT). In a recent study, we reported on three likely HGT candidate genes in the soybean cyst nematode Heterodera glycines, all of which encode secreted candidate effectors with putative functions in the host plant. Hg-GLAND1 is a putative GCN5-related N-acetyltransferase (GNAT), Hg-GLAND13 is a putative invertase (INV), and Hg-GLAND16 is a putative chorismate mutase (CM), and blastp searches of the non-redundant database resulted in highest similarity to bacterial sequences. Here, we searched nematode and non-nematode sequence databases to identify all the nematodes possible that contain these three genes, and to formulate hypotheses about when they most likely appeared in the phylum Nematoda. We then performed phylogenetic analyses combined with model selection tests of alternative models of sequence evolution to determine whether these genes were horizontally acquired from bacteria.ResultsMining of nematode sequence databases determined that GNATs appeared in Hoplolaimina PPN late in evolution, while both INVs and CMs appeared before the radiation of the Hoplolaimina suborder. Also, Hoplolaimina GNATs, INVs and CMs formed well-supported clusters with different rhizosphere bacteria in the phylogenetic trees, and the model selection tests greatly supported models of HGT over descent via common ancestry. Surprisingly, the phylogenetic trees also revealed additional, well-supported clusters of bacterial GNATs, INVs and CMs with diverse eukaryotes and archaea. There were at least eleven and eight well-supported clusters of GNATs and INVs, respectively, from different bacteria with diverse eukaryotes and archaea. Though less frequent, CMs from different bacteria formed supported clusters with multiple different eukaryotes. Moreover, almost all individual clusters containing bacteria and eukaryotes or archaea contained species that inhabit very similar niches.ConclusionsGNATs were horizontally acquired late in Hoplolaimina PPN evolution from bacteria most similar to the saprophytic and plant-pathogenic actinomycetes. INVs and CMs were horizontally acquired from bacteria most similar to rhizobacteria and Burkholderia soil bacteria, respectively, before the radiation of Hoplolaimina. Also, these three gene groups appear to have been frequent subjects of HGT from different bacteria to numerous, diverse lineages of eukaryotes and archaea, which suggests that these genes may confer important evolutionary advantages to many taxa. In the case of Hoplolaimina PPN, this advantage likely was an improved ability to parasitize plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0651-y) contains supplementary material, which is available to authorized users.
Highlights
Hoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT)
Nematode GCN5-related N-acetyltransferase (GNAT), INV and chorismate mutase (CM) homologs may be specific to Hoplolaimina The phylum Nematoda is composed of 12 major clades (Fig. 1a) [55]
Placing the Hoplolaimina Family 7 (FAM7) GNATs with leotiomycete fungi rather than with streptomycete FAM7 GNATs, and placing Hoplolaimina CMs with insect rather than with Burkholderia CMs, resulted in substantially higher scores compared to the unconstrained HGT models (Table 1). These results indicated that the rhizosphere bacteria with which the candidate HGT genes clustered in the phylogenetic analyses (Figs. 4, 5 and 6) are likely modern descendants of the HGT bacterial donors of the FAM7 GNAT, INV and CM genes in Hoplolaimina
Summary
Hoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT). In the phylum Nematoda (Fig. 1a), the plant-parasitic nematodes (PPN) of the suborder Hoplolaimina are among the eukaryotes with the most documented HGT events (reviewed in [2]), especially for HGT from bacterial donors. Large suites of genes that encode plant cell wall-modifying proteins were determined to have been acquired in Hoplolaimina PPN via HGT from different bacterial donors [3]. Genes encoding invertases (INVs; family 32 glycosyl hydrolases) were recently shown to have been acquired in Hoplolaimina PPN from bacteria, and in the potato cyst nematode Globodera pallida, these genes encode functional enzymes that are secreted in the digestive system likely to metabolize hostderived sucrose [6]. Other genes in Hoplolaimina PPN are believed to have bacterial origins, but these hypotheses have not been rigorously tested (reviewed in [2])
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