C.W. Quist

Evolution of Plant Parasitism in the Phylum Nematoda

Within the species-rich and trophically diverse phylum Nematoda, at least four independent major lineages of plant parasites have evolved, and in at least one of these major lineages plant parasitism arose independently multiple times. Ribosomal DNA data, sequence information from nematode-produced, plant cell wall-modifying enzymes, and the morphology and origin of the style(t), a protrusible piercing device used to penetrate the plant cell wall, all suggest that facultative and obligate plant parasites originate from fungivorous ancestors. Data on the nature and diversification of plant cell wall-modifying enzymes point at multiple horizontal gene transfer events from soil bacteria to bacterivorous nematodes resulting in several distinct lineages of fungal or oomycete-feeding nematodes. Ribosomal DNA frameworks with sequence data from more than 2,700 nematode taxa combined with detailed morphological information allow for explicit hypotheses on the origin of agronomically important plant parasites, such as root-knot, cyst, and lesion nematodes.

Disparate gain and loss of parasitic abilities among nematode lineages

Plant parasitism has arisen time and again in multiple phyla, including bacteria, fungi, insects and nematodes. In most of these organismal groups, the overwhelming diversity hampers a robust reconstruction of the origins and diversification patterns of this trophic lifestyle. Being a moderately diversified phylum with ≈ 4,100 plant parasites (15% of total biodiversity) subdivided over four independent lineages, nematodes constitute a major organismal group for which the genesis of plant parasitism could be mapped. Since substantial crop losses worldwide have been attributed to less than 1% of these plant parasites, research efforts are severely biased towards this minority. With the first molecular characterisation of numerous basal and supposedly harmless plant parasites as well as their non-parasitic relatives, we were able to generate a comprehensive molecular framework that allows for the reconstruction of trophic diversification for a complete phylum. In each lineage plant parasites reside in a single taxonomic grouping (family or order), and by taking the coverage of the next lower taxonomic level as a measure for representation, 50, 67, 100 and 85% of the known diversity was included. We revealed distinct gain and loss patterns with regard to plant parasitism per se as well as host exploitation strategies between these lineages. Our map of parasitic nematode biodiversity also revealed an unanticipated time reversal in which the two most ancient lineages showed the lowest level of ecological diversification and vice versa.

Feeding preference as a main determinant of microscale patchiness among terrestrial nematodes

Soil biota are responsible for essential ecosystem services such as carbon storage, nutrient cycling and water retention. However, assessment of the condition of soil biota is hampered by an overwhelming level of diversity. With representatives in all trophic levels of the food web, nematode communities can be used as bioindicators. Accurate assessment of nematode assemblages requires insight into the distribution of specimens with distinct food preferences. With the availability of taxon‐specific quantitative PCR assays, distribution patterns of multiple nematode groups can be investigated simultaneously. Here, microscale patchiness of 45 nematode taxa was studied on 12 sampling sites (each with four adjacent microplots) located on arable fields or semi‐natural grasslands (‘system’), and on marine, river clay or sandy soils (‘soil type’). From each microplot, five composite samples were collected. Contrary to our expectations, an increase in the number of cores per composite sample did not result in more accurate measurements, and apparently the levels of microscale patchiness of the taxa are low compared to what has been reported for oligophagous plant‐parasites. System and soil type did not affect microscale distribution. To investigate the level of patchiness in more detail, detection probability (DP) and variability of abundances were calculated. Common and widespread bacterivorous and fungivorous taxa had DP ≥ 90%, confirming low level of microscale patchiness. With DPs of 40%–70%, predators and most omnivores showed degrees of local clustering. An overview of mean variabilities of abundances is presented that offers insight into how feeding preferences impact the microscale distribution both between and within trophic groups.

Integrating quantitative morphological and qualitative molecular methods to analyse soil nematode community responses to plant range expansion

1. Belowground nematodes are important for soil functioning, as they are ubiquitous and operate at various trophic levels in the soil food web. However, morphological nematode community analysis is time consuming and requires ample training. qPCR-based nematode identification techniques are well available, but high throughput sequencing (HTS) might be more suitable for non-targeted nematode community analysis. 2. We compared effectiveness of qPCR and HTS-based approaches with morphological nematode identification while examining how climate warming-induced plant range expansion may influence belowground nematode assemblages. We extracted nematodes from soil of Centaurea stoebe and C. jacea populations in Slovenia, where both plant species are native, and Germany, where C. stoebe is range expander and C. jacea is native. Half of each nematode sample was identified morphologically and the other half was analysed using targeted qPCR and a novel HTS approach. 3. HTS produced the highest taxonomic resolution of the nematode community. Nematode taxa abundances correlated between the methods. Therefore, especially relative HTS and relative morphological data revealed nearly identical ecological patterns. All methods showed lower numbers of plant feeding nematodes in rhizosphere soils of C. stoebe compared to C. jacea. However, a profound difference was observed between absolute and relative abundance data; both sampling origin and plant species affected relative abundances of bacterivorous nematodes, whereas there was no effect on absolute abundances. 4. Taken together, as HTS correlates with relative analyses of soil nematode communities, while providing highest taxonomic resolution and sample throughput, we propose a combination of HTS with microscopic counting to supplement important quantitative data on soil nematode communities. This provides the most cost-effective, in-depths methodology to study soil nematode community responses to changes in the environment. This methodology will also be applicable to nematode analyses in aquatic systems.