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Intestinal transcriptomes of nematodes: comparison of the parasites Ascaris suum and Haemonchus contortus with the free-living Caenorhabditis elegans.

Yin Y, Martin J, Abubucker S, Scott AL, McCarter JP, Wilson RK, Jasmer DP, Mitreva M - PLoS Negl Trop Dis (2008)

Bottom Line: In contrast, significant conservation of the intestinal gene repertories was also evident, despite the evolutionary distance of approximately 350 million years separating them.Functional characterizations of the IntFam-241 suggested important roles in molecular functions such as protein kinases and proteases, and biological pathways of carbohydrate metabolism, energy metabolism, and translation.Our study has provided novel insights into the nematode intestine and lays foundations for further comparative studies on biology, parasitism, and evolution within the phylum Nematoda.

View Article: PubMed Central - PubMed

Affiliation: Genome Sequencing Center, Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, United States of America. yyin@watson.wustl.edu

ABSTRACT

Background: The nematode intestine is a major organ responsible for nutrient digestion and absorption; it is also involved in many other processes, such as reproduction, innate immunity, stress responses, and aging. The importance of the intestine as a target for the control of parasitic nematodes has been demonstrated. However, the lack of detailed knowledge on the molecular and cellular functions of the intestine and the level of its conservation across nematodes has impeded breakthroughs in this application.

Methods and findings: As part of an extensive effort to investigate various transcribed genomes from Ascaris suum and Haemonchus contortus, we generated a large collection of intestinal sequences from parasitic nematodes by identifying 3,121 A. suum and 1,755 H. contortus genes expressed in the adult intestine through the generation of expressed sequence tags. Cross-species comparisons to the intestine of the free-living C. elegans revealed substantial diversification in the adult intestinal transcriptomes among these species, suggesting lineage- or species-specific adaptations during nematode evolution. In contrast, significant conservation of the intestinal gene repertories was also evident, despite the evolutionary distance of approximately 350 million years separating them. A group of 241 intestinal protein families (IntFam-241), each containing members from all three species, was identified based on sequence similarities. These conserved proteins accounted for approximately 20% of the sampled intestinal transcriptomes from the three nematodes and are proposed to represent conserved core functions in the nematode intestine. Functional characterizations of the IntFam-241 suggested important roles in molecular functions such as protein kinases and proteases, and biological pathways of carbohydrate metabolism, energy metabolism, and translation. Conservation in the core protein families was further explored by extrapolating observable RNA interference phenotypes in C. elegans to their parasitic counterparts.

Conclusions: Our study has provided novel insights into the nematode intestine and lays foundations for further comparative studies on biology, parasitism, and evolution within the phylum Nematoda.

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Related in: MedlinePlus

Putative Secreted or Trans-membrane Proteins in A. suum, H. contortus, and C. elegans.Larger percentages of the putative intestine-enriched genes (Int. Enriched) were predicted to be secreted with signal peptide (SP) or trans-membrane (TM) than either the complete set of intestinal genes (Int. Genes) or the complete set of all available genes (All Genes) in A. suum, H. contortus, and C. elegans.
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pntd-0000269-g002: Putative Secreted or Trans-membrane Proteins in A. suum, H. contortus, and C. elegans.Larger percentages of the putative intestine-enriched genes (Int. Enriched) were predicted to be secreted with signal peptide (SP) or trans-membrane (TM) than either the complete set of intestinal genes (Int. Genes) or the complete set of all available genes (All Genes) in A. suum, H. contortus, and C. elegans.

Mentions: Furthermore, we observed higher levels of diversification in the putative intestine-enriched genes from the three nematodes. Taking into consideration sample size and random sampling fluctuation [28], we identified 150 A. suum, 60 H. contortus, and 247 C. elegans putative intestine-enriched genes based on the “digital” expression levels revealed in EST and SAGE data (at the Poisson distribution-based P-value cutoff of 0.001) (Table S2; Table S3; Table S4). Many of these predicted enrichments suggested unique intestinal functions for the individual species. For example, the group of 60 genes from the blood-feeding H. contortus includes 2 fibrinogen-related proteins that may function as thrombin inhibitors to prevent clotting of ingested blood. Also included are putative enzymes that may be involved in the digestion of hemoglobin, one of the major food sources of blood-feeding parasites, including a serine-type protease, a metallopeptidase, and 13 different cysteine-type proteases that were reported previously [42] (Table S3). Interestingly, a significantly higher percentages of these genes (e.g. 15%-31% higher than all the sampled intestinal genes) encode proteins predicted as secreted or trans-membrane [29] (Figure 2), suggesting that they interact with the extracellular environment. However, 64%, 54%, and 69% of them, from the three species respectively, were distinct from members of the protein families conserved in the intestine of all three nematodes (IntFam-241; see below), indicating that a large portion of these putative intestine-enriched genes are specific to the intestine of individual nematode lineages or species. This further underlines the diversification of intestinal transcriptomes in accommodating the different life styles and feeding patterns among nematodes.


Intestinal transcriptomes of nematodes: comparison of the parasites Ascaris suum and Haemonchus contortus with the free-living Caenorhabditis elegans.

Yin Y, Martin J, Abubucker S, Scott AL, McCarter JP, Wilson RK, Jasmer DP, Mitreva M - PLoS Negl Trop Dis (2008)

Putative Secreted or Trans-membrane Proteins in A. suum, H. contortus, and C. elegans.Larger percentages of the putative intestine-enriched genes (Int. Enriched) were predicted to be secreted with signal peptide (SP) or trans-membrane (TM) than either the complete set of intestinal genes (Int. Genes) or the complete set of all available genes (All Genes) in A. suum, H. contortus, and C. elegans.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2483350&req=5

pntd-0000269-g002: Putative Secreted or Trans-membrane Proteins in A. suum, H. contortus, and C. elegans.Larger percentages of the putative intestine-enriched genes (Int. Enriched) were predicted to be secreted with signal peptide (SP) or trans-membrane (TM) than either the complete set of intestinal genes (Int. Genes) or the complete set of all available genes (All Genes) in A. suum, H. contortus, and C. elegans.
Mentions: Furthermore, we observed higher levels of diversification in the putative intestine-enriched genes from the three nematodes. Taking into consideration sample size and random sampling fluctuation [28], we identified 150 A. suum, 60 H. contortus, and 247 C. elegans putative intestine-enriched genes based on the “digital” expression levels revealed in EST and SAGE data (at the Poisson distribution-based P-value cutoff of 0.001) (Table S2; Table S3; Table S4). Many of these predicted enrichments suggested unique intestinal functions for the individual species. For example, the group of 60 genes from the blood-feeding H. contortus includes 2 fibrinogen-related proteins that may function as thrombin inhibitors to prevent clotting of ingested blood. Also included are putative enzymes that may be involved in the digestion of hemoglobin, one of the major food sources of blood-feeding parasites, including a serine-type protease, a metallopeptidase, and 13 different cysteine-type proteases that were reported previously [42] (Table S3). Interestingly, a significantly higher percentages of these genes (e.g. 15%-31% higher than all the sampled intestinal genes) encode proteins predicted as secreted or trans-membrane [29] (Figure 2), suggesting that they interact with the extracellular environment. However, 64%, 54%, and 69% of them, from the three species respectively, were distinct from members of the protein families conserved in the intestine of all three nematodes (IntFam-241; see below), indicating that a large portion of these putative intestine-enriched genes are specific to the intestine of individual nematode lineages or species. This further underlines the diversification of intestinal transcriptomes in accommodating the different life styles and feeding patterns among nematodes.

Bottom Line: In contrast, significant conservation of the intestinal gene repertories was also evident, despite the evolutionary distance of approximately 350 million years separating them.Functional characterizations of the IntFam-241 suggested important roles in molecular functions such as protein kinases and proteases, and biological pathways of carbohydrate metabolism, energy metabolism, and translation.Our study has provided novel insights into the nematode intestine and lays foundations for further comparative studies on biology, parasitism, and evolution within the phylum Nematoda.

View Article: PubMed Central - PubMed

Affiliation: Genome Sequencing Center, Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, United States of America. yyin@watson.wustl.edu

ABSTRACT

Background: The nematode intestine is a major organ responsible for nutrient digestion and absorption; it is also involved in many other processes, such as reproduction, innate immunity, stress responses, and aging. The importance of the intestine as a target for the control of parasitic nematodes has been demonstrated. However, the lack of detailed knowledge on the molecular and cellular functions of the intestine and the level of its conservation across nematodes has impeded breakthroughs in this application.

Methods and findings: As part of an extensive effort to investigate various transcribed genomes from Ascaris suum and Haemonchus contortus, we generated a large collection of intestinal sequences from parasitic nematodes by identifying 3,121 A. suum and 1,755 H. contortus genes expressed in the adult intestine through the generation of expressed sequence tags. Cross-species comparisons to the intestine of the free-living C. elegans revealed substantial diversification in the adult intestinal transcriptomes among these species, suggesting lineage- or species-specific adaptations during nematode evolution. In contrast, significant conservation of the intestinal gene repertories was also evident, despite the evolutionary distance of approximately 350 million years separating them. A group of 241 intestinal protein families (IntFam-241), each containing members from all three species, was identified based on sequence similarities. These conserved proteins accounted for approximately 20% of the sampled intestinal transcriptomes from the three nematodes and are proposed to represent conserved core functions in the nematode intestine. Functional characterizations of the IntFam-241 suggested important roles in molecular functions such as protein kinases and proteases, and biological pathways of carbohydrate metabolism, energy metabolism, and translation. Conservation in the core protein families was further explored by extrapolating observable RNA interference phenotypes in C. elegans to their parasitic counterparts.

Conclusions: Our study has provided novel insights into the nematode intestine and lays foundations for further comparative studies on biology, parasitism, and evolution within the phylum Nematoda.

Show MeSH
Related in: MedlinePlus