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Comparative genomics of Steinernema reveals deeply conserved gene regulatory networks

ABSTRACT: Parasitism is a major ecological niche for a variety of nematodes. Multiple nematode lineages have specialized as pathogens, including deadly parasites of insects that are used in biological control. We have sequenced and analyzed the draft genomes and transcriptomes of the entomopathogenic nematode Steinernema carpocapsae and four congeners (S. scapterisci, S. monticolum, S. feltiae, and S. glaseri). We used these genomes to establish phylogenetic relationships, explore gene conservation across species, and identify genes uniquely expanded in insect parasites. Protein domain analysis in Steinernema revealed a striking expansion of numerous putative parasitism genes, including certain protease and protease inhibitor families, as well as fatty acid- and retinol-binding proteins. Stage-specific gene expression of some of these expanded families further supports the notion that they are involved in insect parasitism by Steinernema. We show that sets of novel conserved non-coding regulatory motifs are associated with orthologous genes in Steinernema and Caenorhabditis. We have identified a set of expanded gene families that are likely to be involved in parasitism. We have also identified a set of non-coding motifs associated with groups of orthologous genes in Steinernema and Caenorhabditis involved in neurogenesis and embryonic development that are likely part of conserved protein–DNA relationships shared between these two genera.

ORGANISM(S): Caenorhabditis elegans Steinernema carpocapsae Steinernema feltiae

PROVIDER: GSE68588 | GEO | 2015/06/05

SECONDARY ACCESSION(S): PRJNA283145

REPOSITORIES: GEO

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Comparative genomics of Steinernema reveals deeply conserved regulatory networks in nematodes

Project description:Parasitism is a major ecological niche for a variety of nematodes. Multiple nematode lineages have specialized as pathogens, including deadly parasites of insects that are used in biological control. We have sequenced and analyzed the draft genomes and transcriptomes of the entomopathogenic nematode Steinernema carpocapsae and four congeners (S. scapterisci, S. monticolum, S. feltiae, S. glaseri) distantly related to Caenorhabditis elegans. We used these genomes to establish phylogenetic relationships, explore gene conservation across species, identify genes uniquely expanded in insect parasites, and to identify conserved non-coding regulatory motifs that influence similar biological processes. Protein domain analysis of these genomes reveals a striking expansion of numerous putative parasitism genes including certain protease and protease inhibitor families as well as fatty acid- and retinol-binding proteins. We identify rapid evolution and expansion of the important developmental Hox gene cluster and identify novel conserved non-coding regulatory motifs associated with orthologous genes in Steinernema and Caenorhabditis. The deep conservation of the network of non-coding DNA motifs between these two genera for a subset of orthologous genes involved in neurogenesis and embryonic development suggests that a kernel of protein-DNA relationships is conserved through nematode evolution. We analyzed the gene expression of a total of 24 RNA-seq samples from 3 nematode species( S. carpocapsae, S. feltiae, and C. elegans) for comparative analysis. We collected the RNA at four developmental time points (mixed embryo, L1, infective juvenile/dauer, young adult) for each species in replicates.

2015-06-05 | E-GEOD-68588 | biostudies-arrayexpress

Hybrid assembly of the genome of the entomopathogenic nematode Steinernema carpocapsae identifies the X-chromosome.

Project description:Entomopathogenic nematodes from the genus Steinernema are lethal insect parasites that quickly kill their insect hosts with the help of their symbiotic bacteria. Steinernema carpocapsae is one of the most studied entomopathogens due to its broad lethality to diverse insect species and its effective commercial use as a biological control agent for insect pests, as well as a genetic model for studying parasitism, pathogenesis, and symbiosis. In this study, we used long-reads from the Pacific Biosciences platform and BioNano Genomics Irys system to assemble the best genome of S. carpocapsae ALL strain to date, comprising 84.5 Mb in 16 scaffolds, with an N50 of 7.36Mb. The largest scaffold, with 20.9Mb, was identified as chromosome X based on sex-specific genome sequencing. The high level of contiguity allowed us to characterize gene density, repeat content, and GC content. RNA-seq data from 17 developmental stages, spanning from embryo to adult, were used to predict 30,957 gene models. Using this new genome, we performed a macrosyntenic analysis to Caenorhabditis elegans and Pristionchus pacificus and found S. carpocapsae’s chromosome X to be primarily orthologous to C. elegans’ and P. pacificus’ chromosome II and IV. We also investigated the expansion of protein families and gene expression differences between male and female stage nematodes. This new genome and more accurate set of annotations provide a foundation for new comparative genomic and gene expression studies within the Steinernema clade and across the Nematode phylum.

2019-03-06 | GSE127823 | GEO

Comparative transcriptomics of Steinernema and Caenorhabditis single embryos reveals gene expression divergence during early embryogenesis

Project description:Abstract: Cells express distinct sets of genes in a precise spatio-temporal manner during embryonic development. There is a wealth of information about embryonic development in C. elegans, but much less is known about embryonic development at the molecular level in nematodes from other taxa. We are interested in insect pathogenic nematodes from the genus Steinernema as models of parasitism and symbiosis as well as a satellite model for evolution in comparison to C. elegans. We sequenced the transcriptomes of single embryos of two Steinernema species and two Caenorhabditis species at eleven specific stages during embryonic development for comparative analysis. We found that zygotic transcription initiates at different developmental stages in each species, with the Steinernema species initiating transcription at earlier developmental stages than Caenorhabditis. We found that ortholog expression conservation during development is highest at the later embryonic stages than at the earlier ones. Moreover, we found that the components of the neddylation pathway are highly upregulated during Steinernema early embryonic development contributing further to these early differences seen between the genera at the post-translational level. The surprisingly higher conservation of orthologous gene expression in later embryonic stages strongly suggests a funnel-shaped model of developmental gene expression divergence in nematodes. This work provides novel insight into embryonic development across distantly related nematode species and demonstrates that the mechanisms controlling early development are more diverse than previously thought at both the transcriptional and post-translational level.

2017-09-26 | GSE86381 | GEO

Steinernema carpocapsae Breton small RNA sequencing insect in vitro simulation system, from "The genome, transcriptome, and proteome of the nematode Steinernema carpocapsae: evolutionary signatures of a pathogenic lifestyle"

Project description:We report small RNA sequencing of the entomopathogenic nematode Steinernema carpocapsae. The nematodes were grown in liquid culture in homogenates of pig kidney/fat and infective juveniles were gathered. Then Galleria mellonella insect haemolymph was added to simulate insect infection, control nematodes weren't added haemolymph. Nematodes were collected after two hours after haemolymph addition.

2016-09-05 | GSE85256 | GEO

2016-09-05 | E-GEOD-85256 | biostudies-arrayexpress

Activated entomopathogenic nematode infective juveniles release lethal venom proteins

Project description:Entomopathogenic nematodes (EPNs) are unique parasitic nematodes due to their symbiosis with entomopathogenic bacteria and their ability to kill insect hosts quickly after infection. Although it has been widely believed that EPNs rely on their bacterial partners for killing insect hosts, compelling evidence from previous studies challenges this model. We developed an improved method of activating millions of Steinernema carpocapsae infective juveniles (IJs) in vitro to harvest excreted/secreted (ES) proteins for bioactivity tests and proteomics analysis. We found that a low dose of the ES proteins from early activated nematodes is lethal to Drosophila melanogaster adults within 2-6 hours. We analyzed the protein composition of this venom using mass spectrometry and identified 472 proteins. Many of these venom proteins share high homology with those of vertebrate-parasitic nematodes. Among many different families of proteins found in the venom, proteases and protease inhibitors are especially abundant. Some toxin-related proteins such as Shk domain-containing proteins were also detected. We further analyzed the transcriptomes of individual non-activated IJs and nematodes that were activated in vitro and in vivo, which revealed a dramatic shift in gene expression during IJ activation. By comparing the whole transcriptomes and the genes encoding venom proteins between the in vitro and in vivo activated nematodes, we confirmed that the in vitro activation is a good approximation of the in vivo process. In summary, our findings strongly support a new model that S. carpocapsae and likely other Steinernema EPNs have a more active role in contributing to the pathogenicity of the nematode-bacterium complex than simply relying on their symbiotic bacteria. Furthermore, we propose that EPNs are a good model system for investigating vertebrate- and human-parasitic nematodes, especially regarding the function of ES products.

2017-03-27 | GSE89961 | GEO

The Effect of Temperature Conditioning (9°C and 20°C) on the Proteome of Steinernema carpocapsae and Heterorhabditis megidis Infective Juveniles

Project description:Entomopathogenic nematodes (Rhabditida; Steinernematidae and Heterorhabditidae) are insect parasites which are of economic importance due to their use as biocontrol agents. The third larval stage, infective juveniles (IJs) leave the natal host and move in the soil to locate a new insect host. Both families are associated with mutualistic bacteria, which are released into the haemolymph of the host insect, killing the insect and providing nutrition for nematode development and reproduction, and are thus categorised as entomopathogenic nematodes. Similarities between these two families are due to convergent evolution associated with this lifestyle, rather than common ancestry. Heterorhabditids are closely related to the vertebrate parasites Strongylida (Adams and Nguyen, 2002) and to Caenorhabditis elegans, whereas steinernematids are more closely related to Strongyloididae. The IJ stage of parasitic nematodes is analogous to the dauer stage of C. elegans; both are developmentally arrested, stress resistant stages that disperse to colonise new hosts or food resources, respectively. By investigating the molecular mechanisms and consequences of temperature acclimation and aging in EPN IJs, insights into survival and the changes induced by low temperature exposure may be gained. Label free quantitative (LFQ) massspectrometery-based proteomics facilitates the identification and quantification of thousands of proteins in a single run. Such data allows for the comparison of the proteomes of EPN IJs after conditioning via gene ontology mapping and functional enrichment analysis. Understanding how the IJ proteome is affected by temperature and aging can provide a molecular basis for the wide array of phenotypes and behaviours these organisms may adopt. This study aims to provide proteomic data which may elucidate the molecular mechanisms underlying the phenotypic plasticity which EPN IJs of two distantly related species exhibit.

2022-03-27 | PXD027608 | Pride

Excreted-Secreted Proteins from activated infective junveiles of the entomopathogenic nematode Steinernema feltiae

Project description:Entomopathogenic nematode infective juveniles activate when they infect a host and begin releasing excreted-secreted products. These are the excreted-secreted proteins detected by mass spec from activated Steinernema feltiae infective juveniles. The infective juveniles were activated in vitro by exposure to insect-host tissue for 6 hours.

2018-10-02 | MSV000082993 | MassIVE

An extracellular Argonaute protein mediates export of repeat-associated small RNAs into vesicles in parasitic nematodes

Project description:Mobile small RNAs are an integral component of the arms race between plants and fungal parasites, and several studies suggest microRNAs could similarly operate between parasitic nematodes and their animal hosts. However, whether and how specific sequences are selected for export by parasites is unknown. Here we describe a specific Argonaute protein (exWAGO) that is secreted in extracellular vesicles (EVs) released by the gastrointestinal nematode Heligmosomodies bakeri, at multiple copies per EV. Phylogenetic and gene expression analyses demonstrate exWAGO is highly conserved and abundantly expressed in related parasites, including the human hookworm and proteomic analyses confirm this is the only Argonaute secreted by rodent parasites. In contrast, exWAGO orthologues in species from the free-living genus Caenorhabditis are highly diverged. By sequencing multiple small RNA libraries, we determined that the most abundant small RNAs released from the nematode parasite are not microRNAs but rather secondary small interfering RNAs (siRNAs) that are produced by RNA-dependent RNA Polymerases. We further identify distinct evolutionary properties of the siRNAs resident in free-living or parasitic nematodes versus those exported in EVs by the parasite and show that the latter are specifically associated with exWAGO. Together this work identifies an Argonaute protein as a mediator of RNA export and suggests rhabditomorph nematode parasites may have co-opted a novel nematode-unique pathway to communicate with their hosts.

2019-02-21 | GSE117169 | GEO

RNA-Sequencing analysis of the Drosophila transcriptomic response to infection by entomopathogenic nematodes and their mutualistic bacteria

Project description:We report the application of next generation RNA sequencing to analyze the transcriptional response of Drosophila adult flies to infection by the insect pathogenic nematodes Heterorhabditis bacteriophora and their mutualistic bacteria Photorhabdus luminescens, either separately or together. We find that Heterorhabditis and Photorhabdus differentially modulate a large number of genes, many of which participate in metabolic functions, stress responses, repression of gene transcription and neuronal activities. We have also identified Drosophila genes with potential role in nematode recognition and others with putative anti-nematode properties. These findings generate novel insights into how the host immune function is shaped to respond against nematode parasites and their associated bacteria.

2015-09-12 | GSE61466 | GEO

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