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. 2013 Feb 22;14:118.
doi: 10.1186/1471-2164-14-118.

Transcriptome Analyses Reveal Protein and Domain Families That Delineate Stage-Related Development in the Economically Important Parasitic Nematodes, Ostertagia Ostertagi and Cooperia Oncophora

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Transcriptome Analyses Reveal Protein and Domain Families That Delineate Stage-Related Development in the Economically Important Parasitic Nematodes, Ostertagia Ostertagi and Cooperia Oncophora

Esley Heizer et al. BMC Genomics. .
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Abstract

Background: Cooperia oncophora and Ostertagia ostertagi are among the most important gastrointestinal nematodes of cattle worldwide. The economic losses caused by these parasites are on the order of hundreds of millions of dollars per year. Conventional treatment of these parasites is through anthelmintic drugs; however, as resistance to anthelmintics increases, overall effectiveness has begun decreasing. New methods of control and alternative drug targets are necessary. In-depth analysis of transcriptomic data can help provide these targets.

Results: The assembly of 8.7 million and 11 million sequences from C. oncophora and O. ostertagi, respectively, resulted in 29,900 and 34,792 transcripts. Among these, 69% and 73% of the predicted peptides encoded by C. oncophora and O. ostertagi had homologues in other nematodes. Approximately 21% and 24% were constitutively expressed in both species, respectively; however, the numbers of transcripts that were stage specific were much smaller (~1% of the transcripts expressed in a stage). Approximately 21% of the transcripts in C. oncophora and 22% in O. ostertagi were up-regulated in a particular stage. Functional molecular signatures were detected for 46% and 35% of the transcripts in C. oncophora and O. ostertagi, respectively. More in-depth examinations of the most prevalent domains led to knowledge of gene expression changes between the free-living (egg, L1, L2 and L3 sheathed) and parasitic (L3 exsheathed, L4, and adult) stages. Domains previously implicated in growth and development such as chromo domains and the MADF domain tended to dominate in the free-living stages. In contrast, domains potentially involved in feeding such as the zinc finger and CAP domains dominated in the parasitic stages. Pathway analyses showed significant associations between life-cycle stages and peptides involved in energy metabolism in O. ostertagi whereas metabolism of cofactors and vitamins were specifically up-regulated in the parasitic stages of C. oncophora. Substantial differences were observed also between Gene Ontology terms associated with free-living and parasitic stages.

Conclusions: This study characterized transcriptomes from multiple life stages from both C. oncophora and O. ostertagi. These data represent an important resource for studying these parasites. The results of this study show distinct differences in the genes involved in the free-living and parasitic life cycle stages. The data produced will enable better annotation of the upcoming genome sequences and will allow future comparative analyses of the biology, evolution and adaptation to parasitism in nematodes.

Figures

Figure 1
Figure 1
Distribution of protein homologues in free-living nematodes, Strongylida parasites, and Non-Strongylida parasites. The percent of homologues in each of the three databases as well as the overlap between the databases is shown. (A). C. oncophora; (B). O. ostertagi. For species included in each of the three databases please see the Materials and Methods.
Figure 2
Figure 2
Transcript expression in different developmental stages. This figure represents the number of transcripts expressed in each stage and the percent of those transcripts that are constitutively-expressed in C. oncophora (A) and O. ostertagi (B). (C) C. oncophora and (D) O. ostertagi depict the number of transcripts up-regulated, down-regulated and specific to a given stage.
Figure 3
Figure 3
GO term associations with transcripts expressed in each stage. For each phase of the life cycle (free-living or parasitic) several prevalent GO terms are listed. * indicates a given term is significantly-enriched in that life cycle stage (p < 0.05). (A) C. oncophora; (B) O. ostertagi.
Figure 4
Figure 4
Significantly-enriched (p< 0.05) InterPro domains in the free-living (egg, L1, L2, L3sh) or parasitic (L3ex, L4 and adult) stages of (A) C. oncophora and (B) O. ostertagi.
Figure 5
Figure 5
Clustering of stages based upon the number of transcripts in a stage containing a specific InterPro domain. (A) C. oncophora; (B) O.ostertagi. A lower-range scale (0 to 3+) was used to better illustrate the similarities and differences between the stages.
Figure 6
Figure 6
Comparison of phenotype distribution between RNAi-surveyed C. elegans genes, and C. onchophora and O. ostertagi homologues to C. elegans genes with similar phenotypes. (A). The percent of C. oncophora peptides encoded by transcripts expressed in free-living stages (egg, L1, L2 and L3sh) with homologs to C. elegans proteins with various RNAi phenotypes. (B). The percent of O. ostertagi peptides encoded by transcripts expressed in parasitic stages (L3ex, L4 and adult) with homologs to C. elegans proteins with various RNAi phenotypes. “*” indicates that for a specific RNAi phenotype, significantly more (p < 0.05) peptides in either C. oncophora or O. ostertagi exhibited that phenotype than did C. elegans.
Figure 7
Figure 7
Distribution of KEGG categories associated with up-regulated transcripts. The number of up-regulated transcripts in free-living and parasitic life stages associated with KEGG categories is compared in (A) C. oncophora and (B) O. ostertagi. * indicates significance (p <0.05).

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