Signal sequence analysis of expressed sequence tags from the nematode Nippostrongylus brasiliensisand the evolution of secreted proteins in parasites

Harcus, Yvonne; Parkinson, John; Fernández, Cecilia; Daub, Jennifer; Selkirk, Murray E.; Blaxter, Mark; Maizels, Rick M.

doi:10.1186/gb-2004-5-6-r39

Cited by 59 publications

(21 citation statements)

References 64 publications

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“…These results therefore suggest that secreted proteins in Echinococcus are less evolutionarily conserved than non-secreted proteins. However, these differences in conservation are much less dramatic than previously reported for N. brasiliensis , in which 48.9% of signal positive peptides could be described as genus-specific compared to 26.8% for the dataset overall [64].…”

Section: Resultscontrasting

confidence: 69%

“…Previously, in a transcriptomic study of the parasitic nematode Nippostrongylus brasiliensis , we noted that signal sequence-bearing proteins showed reduced evolutionary conservation [64]. This observation was confirmed and extended in a subsequent study: parasitic nematodes were found to have a greater proportion of novel, secreted proteins than free-living ones [65].…”

Section: Resultsmentioning

confidence: 53%

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A Transcriptomic Analysis of Echinococcus granulosus Larval Stages: Implications for Parasite Biology and Host Adaptation

et al. 2012

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BackgroundThe cestode Echinococcus granulosus - the agent of cystic echinococcosis, a zoonosis affecting humans and domestic animals worldwide - is an excellent model for the study of host-parasite cross-talk that interfaces with two mammalian hosts. To develop the molecular analysis of these interactions, we carried out an EST survey of E. granulosus larval stages. We report the salient features of this study with a focus on genes reflecting physiological adaptations of different parasite stages.Methodology/Principal FindingsWe generated ∼10,000 ESTs from two sets of full-length enriched libraries (derived from oligo-capped and trans-spliced cDNAs) prepared with three parasite materials: hydatid cyst wall, larval worms (protoscoleces), and pepsin/H+-activated protoscoleces. The ESTs were clustered into 2700 distinct gene products. In the context of the biology of E. granulosus, our analyses reveal: (i) a diverse group of abundant long non-protein coding transcripts showing homology to a middle repetitive element (EgBRep) that could either be active molecular species or represent precursors of small RNAs (like piRNAs); (ii) an up-regulation of fermentative pathways in the tissue of the cyst wall; (iii) highly expressed thiol- and selenol-dependent antioxidant enzyme targets of thioredoxin glutathione reductase, the functional hub of redox metabolism in parasitic flatworms; (iv) candidate apomucins for the external layer of the tissue-dwelling hydatid cyst, a mucin-rich structure that is critical for survival in the intermediate host; (v) a set of tetraspanins, a protein family that appears to have expanded in the cestode lineage; and (vi) a set of platyhelminth-specific gene products that may offer targets for novel pan-platyhelminth drug development.Conclusions/SignificanceThis survey has greatly increased the quality and the quantity of the molecular information on E. granulosus and constitutes a valuable resource for gene prediction on the parasite genome and for further genomic and proteomic analyses focused on cestodes and platyhelminths.

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Section: Resultscontrasting

confidence: 69%

Section: Resultsmentioning

confidence: 53%

A Transcriptomic Analysis of Echinococcus granulosus Larval Stages: Implications for Parasite Biology and Host Adaptation

et al. 2012

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“…TUGs predicted to be part of gene families that arose in the last common ancestor of Nematoda or to be novel to A. crassus contained the highest proportion of genes predicted to have secretory signal peptides. This confirms observations made in a Nippostrongylus brasiliensis [71], where secreted and surface proteins were less conserved. Analysis of dn/ds (see below) across conservation categories favors the hypothesis of rapid evolution in proteins with more restricted phylogenetic origins.…”

Section: Discussionsupporting

confidence: 91%

The transcriptome of the invasive eel swimbladder nematode parasite Anguillicola crassus

et al. 2013

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BackgroundAnguillicola crassus is an economically and ecologically important parasitic nematode of eels. The native range of A. crassus is in East Asia, where it infects Anguilla japonica, the Japanese eel. A. crassus was introduced into European eels, Anguilla anguilla, 30 years ago. The parasite is more pathogenic in its new host than in its native one, and is thought to threaten the endangered An. anguilla across its range. The molecular bases for the increased pathogenicity of the nematodes in their new hosts is not known.ResultsA reference transcriptome was assembled for A. crassus from Roche 454 pyrosequencing data. Raw reads (756,363 total) from nematodes from An. japonica and An. anguilla hosts were filtered for likely host contaminants and ribosomal RNAs. The remaining 353,055 reads were assembled into 11,372 contigs of a high confidence assembly (spanning 6.6 Mb) and an additional 21,153 singletons and contigs of a lower confidence assembly (spanning an additional 6.2 Mb). Roughly 55% of the high confidence assembly contigs were annotated with domain- or protein sequence similarity derived functional information. Sequences conserved only in nematodes, or unique to A. crassus were more likely to have secretory signal peptides. Thousands of high quality single nucleotide polymorphisms were identified, and coding polymorphism was correlated with differential expression between individual nematodes. Transcripts identified as being under positive selection were enriched in peptidases. Enzymes involved in energy metabolism were enriched in the set of genes differentially expressed between European and Asian A. crassus.ConclusionsThe reference transcriptome of A. crassus is of high quality, and will serve as a basis for future work on the invasion biology of this important parasite. The polymorphisms identified will provide a key tool set for analysis of population structure and identification of genes likely to be involved in increased pathogenicity in European eel hosts. The identification of peptidases under positive selection is a first step in this programme.

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“…Some fraction of the remaining 310 contigs may also be forward and reverse pairs, particularly those containing a large and similar number of ESTs, but we have conservatively treated each as a separate transcript (with the exception of Bp0008, which we interpret as an incompletely spliced product of the same gene as Bp0417). The redundancy of the library (which decreases to 4.7 without the rRNA transcripts and incompletely spliced EST), is higher than libraries of other invertebrate metazoans, such as the copepod Tigriopus japonicus (2.62 [35]), the cladoceran Daphnia magna (2.44 [36]), the cnidarian Cyanea capillata (2.11[37]), and the nematode Nippostrongylus brasiliensis (1.66[38]). The reason for such high redundancy is unclear; however, we hypothesize that the expression of many genes may have been depressed during starvation.…”

Section: Discussionmentioning

confidence: 96%

Analysis of Expressed Sequence Tags of the Cyclically Parthenogenetic Rotifer Brachionus plicatilis

et al. 2007

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BackgroundRotifers are among the most common non-arthropod animals and are the most experimentally tractable members of the basal assemblage of metazoan phyla known as Gnathifera. The monogonont rotifer Brachionus plicatilis is a developing model system for ecotoxicology, aquatic ecology, cryptic speciation, and the evolution of sex, and is an important food source for finfish aquaculture. However, basic knowledge of the genome and transcriptome of any rotifer species has been lacking.Methodology/Principal FindingsWe generated and partially sequenced a cDNA library from B. plicatilis and constructed a database of over 2300 expressed sequence tags corresponding to more than 450 transcripts. About 20% of the transcripts had no significant similarity to database sequences by BLAST; most of these contained open reading frames of significant length but few had recognized Pfam motifs. Sixteen transcripts accounted for 25% of the ESTs; four of these had no significant similarity to BLAST or Pfam databases. Putative up- and downstream untranslated regions are relatively short and AT rich. In contrast to bdelloid rotifers, there was no evidence of a conserved trans-spliced leader sequence among the transcripts and most genes were single-copy.Conclusions/SignificanceDespite the small size of this EST project it revealed several important features of the rotifer transcriptome and of individual monogonont genes. Because there is little genomic data for Gnathifera, the transcripts we found with no known function may represent genes that are species-, class-, phylum- or even superphylum-specific; the fact that some are among the most highly expressed indicates their importance. The absence of trans-spliced leader exons in this monogonont species contrasts with their abundance in bdelloid rotifers and indicates that the presence of this phenomenon can vary at the subphylum level. Our EST database provides a relatively large quantity of transcript-level data for B. plicatilis, and more generally of rotifers and other gnathiferan phyla, and can be browsed and searched at gmod.mbl.edu.

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Signal sequence analysis of expressed sequence tags from the nematode Nippostrongylus brasiliensisand the evolution of secreted proteins in parasites

Cited by 59 publications

References 64 publications

A Transcriptomic Analysis of Echinococcus granulosus Larval Stages: Implications for Parasite Biology and Host Adaptation

A Transcriptomic Analysis of Echinococcus granulosus Larval Stages: Implications for Parasite Biology and Host Adaptation

The transcriptome of the invasive eel swimbladder nematode parasite Anguillicola crassus

Analysis of Expressed Sequence Tags of the Cyclically Parthenogenetic Rotifer Brachionus plicatilis

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