Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods

Background: Although molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods. To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. In addition, we performed retrograde staining of nerves in the onychophoran Euperipatoides rowelli in order to compare the serial locations of motor neurons within the nervous system relative to the appendages they serve in arthropods, tardigrades and onychophorans. Results: Contrary to a previous report from a Macrobiotus species, our immunocytochemical and electron microscopic data revealed contralateral fibres and bundles of neurites in each trunk ganglion of three tardigrade species, including Macrobiotus cf. harmsworthi, Paramacrobiotus richtersi and Hypsibius dujardini. Moreover, we identified additional, extra-ganglionic commissures in the interpedal regions bridging the paired longitudinal connectives. Within the ganglia we found serially repeated sets of serotonin- and RFamid-like immunoreactive neurons. Furthermore, our data show that the trunk ganglia of tardigrades, which include the somata of motor neurons, are shifted anteriorly with respect to each corresponding leg pair, whereas no such shift is evident in the arrangement of motor neurons in the onychophoran nerve cords. Conclusions: Taken together, these data reveal three major correspondences between the segmental ganglia of tardigrades and arthropods, including (i) contralateral projections and commissures in each ganglion, (ii) segmentally repeated sets of immunoreactive neurons, and (iii) an anteriorly shifted (parasegmental) position of ganglia. These correspondences support the homology of segmental ganglia in tardigrades and arthropods, suggesting that these structures were either lost in Onychophora or, alternatively, evolved in the tardigrade/arthropod lineage

Foraging theory and partial consumption in a tardigrade-nematode system

Hohberg K, Traunspurger W. Foraging theory and partial consumption in a tardigrade-nematode system. BEHAVIORAL ECOLOGY. 2009;20(4):884-890.We investigated foraging behavior of a carnivorous eutardigrade, Macrobiotus richtersi, living in soil or fresh water sediments, where the distribution of nematode prey is heterogeneous and where, consequently, the value of information about prey availability should be high. We directly observed diet choice in various mixtures of 2 size classes of nematodes Acrobeloides nanus, A1 (small prey) and A2 (large prey), differing in profitability (biomass divided by handling time) but not in digestive quality. At various prey densities of A2, we measured how much of each prey item was consumed as a function of search time. Additionally, we derived cumulative biomass uptake rates per single A2 prey from 154 complete feeding acts, and we used the marginal value theorem (MVT) to predict optimal residence time and prey exploitation as a function of environmental quality and search time. Macrobiotus richtersi did not preferentially select the more profitable size class A2 but increased its biomass uptake rate by modifying the amount consumed per prey item (partial consumption): when encounter rates were high and there were more high-quality prey, the tardigrade abandoned food more quickly and consumed less biomass per captured prey. We conclude that 1) hungry tardigrades under food-rich or food-limited conditions maximize biomass gain according to MVT and 2) tardigrades differentiate at least 2 prey situations, high supply (at high encounter rates) and low supply (at moderate and low prey densities). 3) Partial consumption, performed under food-rich conditions or by a satiated predator, leads to a reduction of prey numbers up to 3 times as much as under food-poor conditions

The D3-D5 region of large subunit ribosomal DNA provides good resolution of German limnic and terrestrial nematode communities

Reliable and well-developed DNA barcode databases are indispensable for the identification of microscopic life. However, effectiveness of molecular barcoding in identifying terrestrial specimens, and nematodes in particular, has received little attention. In this study, ca 600 ribosomal large subunit DNA fragments (D3-D5 region) were successfully amplified for 79 limnic and terrestrial nematode species sampled at 147 locations across Germany. Distinctive DNA motifs in the LSU region were identified in 80% of all species examined. For 13 supposedly single morphospecies, 2-7 LSU barcode groups were detected with a wide range of intraspecific variations (0.09-7.9%). This region seems to be more suitable for the assessment of limno-terrestrial nematode diversity than the frequently used mitochondrial gene COI, as amplification success of the latter fragment is low for several nematode species. Our reference database for nematodes may serve as a starting point for applied and fundamental studies for these ubiquitous, ecologically highly relevant, organisms

The D3-D5 region of large subunit ribosomal DNA provides good resolution of German limnic and terrestrial nematode communities

Schenk J, Hohberg K, Helder J, Ristau K, Traunspurger W. The D3-D5 region of large subunit ribosomal DNA provides good resolution of German limnic and terrestrial nematode communities. Nematology. 2017;19(7):821-837

Shotgun metagenomics of soil invertebrate communities reflects taxonomy, biomass, and reference genome properties

Metagenomics – shotgun sequencing of all DNA fragments from a community DNA extract – is routinely used to describe the composition, structure, and function of microorganism communities. Advances in DNA sequencing and the availability of genome databases increasingly allow the use of shotgun metagenomics on eukaryotic communities. Metagenomics offers major advances in the recovery of biomass relationships in a sample, in comparison to taxonomic marker gene-based approaches (metabarcoding). However, little is known about the factors which influence metagenomics data from eukaryotic communities, such as differences among organism groups, the properties of reference genomes, and genome assemblies. We evaluated how shotgun metagenomics records composition and biomass in artificial soil invertebrate communities at different sequencing efforts. We generated mock communities of controlled biomass ratios from 28 species from all major soil mesofauna groups: mites, springtails, nematodes, tardigrades, and potworms. We shotgun sequenced these communities and taxonomically assigned them with a database of over 270 soil invertebrate genomes. We recovered over 95% of the species, and observed relatively high false-positive detection rates. We found strong differences in reads assigned to different taxa, with some groups (e.g., springtails) consistently attracting more hits than others (e.g., enchytraeids). Original biomass could be predicted from read counts after considering these taxon-specific differences. Species with larger genomes, and with more complete assemblies, consistently attracted more reads than species with smaller genomes. The GC content of the genome assemblies had no effect on the biomass–read relationships. Results were similar among different sequencing efforts. The results show considerable differences in taxon recovery and taxon specificity of biomass recovery from metagenomic sequence data. The properties of reference genomes and genome assemblies also influence biomass recovery, and they should be considered in metagenomic studies of eukaryotes. We show that low- and high-sequencing efforts yield similar results, suggesting high cost-efficiency of metagenomics for eukaryotic communities. We provide a brief roadmap for investigating factors which influence metagenomics-based eukaryotic community reconstructions. Understanding these factors is timely as accessibility of DNA sequencing and momentum for reference genomes projects show a future where the taxonomic assignment of DNA from any community sample becomes a reality.publishe

The soil food web ontology: Aligning trophic groups, processes, resources, and dietary traits to support food-web research

International audienceAlthough soil ecology has benefited from recent advances in describing the functional and trophic traits of soil organisms, data reuse for large-scale soil food-web reconstructions still faces challenges. These obstacles include: (1) most data on the trophic interactions and feeding behaviour of soil organisms being scattered across disparate repositories, without well-established standard for describing and structuring trophic datasets; (2) the existence of various competing terms, rather than consensus, to delineate feeding-related concepts such as diets, trophic groups, feeding processes, resource types, leading to ambiguities that hinder meaningful data integration from different studies; (3) considerable divergence in the trophic classification of numerous soil organisms, or even the lack of such classifications, leading to discrepancies in the resolution of reconstructed food webs and complicating the reuse and comparison of food-web models within synthetic studies. To address these issues, we introduce the Soil Food Web Ontology, a novel formal conceptual framework designed to foster agreement on the trophic ecology of soil organisms. This ontology represents a collaborative and ongoing endeavour aimed at establishing consensus and formal definitions for the array of concepts relevant to soil trophic ecology. Its primary objective is to enhance the accessibility, interpretation, combination, reuse, and automated processing of trophic data. By harmonising the terminology and fundamental principles of soil trophic ecology, we anticipate that the Soil Food Web Ontology will improve knowledge management within the field. It will help soil ecologists to better harness existing information regarding the feeding behaviours of soil organisms, facilitate more robust trophic classifications, streamline the reconstruction of soil food webs, and ultimately render food-web research more inclusive, reusable and reproducible

The MetaInvert soil invertebrate genome resource provides insights into below-ground biodiversity and evolution

Abstract Soil invertebrates are among the least understood metazoans on Earth. Thus far, the lack of taxonomically broad and dense genomic resources has made it hard to thoroughly investigate their evolution and ecology. With MetaInvert we provide draft genome assemblies for 232 soil invertebrate species, representing 14 common groups and 94 families. We show that this data substantially extends the taxonomic scope of DNA- or RNA-based taxonomic identification. Moreover, we confirm that theories of genome evolution cannot be generalised across evolutionarily distinct invertebrate groups. The soil invertebrate genomes presented here will support the management of soil biodiversity through molecular monitoring of community composition and function, and the discovery of evolutionary adaptations to the challenges of soil conditions

A global database of soil nematode abundance and functional group composition

As the most abundant animals on earth, nematodes are a dominant component of the soil community. They play critical roles in regulating biogeochemical cycles and vegetation dynamics within and across landscapes and are an indicator of soil biological activity. Here, we present a comprehensive global dataset of soil nematode abundance and functional group composition. This dataset includes 6,825 georeferenced soil samples from all continents and biomes. For geospatial mapping purposes these samples are aggregated into 1,933 unique 1-km pixels, each of which is linked to 73 global environmental covariate data layers. Altogether, this dataset can help to gain insight into the spatial distribution patterns of soil nematode abundance and community composition, and the environmental drivers shaping these patterns.Peer reviewe