Limits...
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.

Show MeSH

Related in: MedlinePlus

Protein Families in the Adult Intestine from A. suum, H. contortus, and C. elegans.In total, 5,587 intestinal protein families (IntFam) were built from the complete set of 9,918 translated intestinal genes sampled from the three species. Forty-one percent of all the intestinal genes were grouped into 910 multiple-species IntFam groups; 2,024 genes, including 752 from A. suum, 455 from H. contortus, and 817 from C. elegans, were found in a group of 241 families (IntFam-241) containing members from all three intestines. The IntFam-241 families likely represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even to Nematoda, they are thus referred as the “core” IntFam-241 group.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2483350&req=5

pntd-0000269-g004: Protein Families in the Adult Intestine from A. suum, H. contortus, and C. elegans.In total, 5,587 intestinal protein families (IntFam) were built from the complete set of 9,918 translated intestinal genes sampled from the three species. Forty-one percent of all the intestinal genes were grouped into 910 multiple-species IntFam groups; 2,024 genes, including 752 from A. suum, 455 from H. contortus, and 817 from C. elegans, were found in a group of 241 families (IntFam-241) containing members from all three intestines. The IntFam-241 families likely represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even to Nematoda, they are thus referred as the “core” IntFam-241 group.

Mentions: To compare the intestinal transcriptomes of A. suum, H. contortus, and C. elegans in a single analysis, we built protein families from the complete set of 9,918 translated intestinal genes combined from the three nematodes. A total of 5,587 intestinal protein families (IntFam) were identified conservatively based on sequence similarities by MCL clustering [31] (Figure 4). Proteins assigned into the same protein family contain putative homologous or orthologous matches among the three species. Both diversification and conservation of the intestinal transcriptomes was obvious at the protein family level in this 3-species comparison. A total of 59% of all the sampled intestinal genes were members of the protein families containing proteins from only one nematode (Figure 4). Although the assignments for many of these single-species families are likely to change when more complete intestinal gene repertories become available, this group includes the genes contributing to the unique intestinal features in each species. The remaining 41% of the intestinal genes formed 910 multi-species protein families; they are conserved in the intestine of at least two nematodes. Among these multi-species families, 241 had members from all three species, accounting for ∼20% of all the intestinal genes under investigation (Figure 4). Given the differences in life styles and feeding patterns among the three nematodes, we propose that these 241 intestinal protein families represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even across the Nematoda. Therefore, we referred to them as the “core” IntFam-241 group.


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)

Protein Families in the Adult Intestine from A. suum, H. contortus, and C. elegans.In total, 5,587 intestinal protein families (IntFam) were built from the complete set of 9,918 translated intestinal genes sampled from the three species. Forty-one percent of all the intestinal genes were grouped into 910 multiple-species IntFam groups; 2,024 genes, including 752 from A. suum, 455 from H. contortus, and 817 from C. elegans, were found in a group of 241 families (IntFam-241) containing members from all three intestines. The IntFam-241 families likely represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even to Nematoda, they are thus referred as the “core” IntFam-241 group.
© Copyright Policy
Related In: Results  -  Collection

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

pntd-0000269-g004: Protein Families in the Adult Intestine from A. suum, H. contortus, and C. elegans.In total, 5,587 intestinal protein families (IntFam) were built from the complete set of 9,918 translated intestinal genes sampled from the three species. Forty-one percent of all the intestinal genes were grouped into 910 multiple-species IntFam groups; 2,024 genes, including 752 from A. suum, 455 from H. contortus, and 817 from C. elegans, were found in a group of 241 families (IntFam-241) containing members from all three intestines. The IntFam-241 families likely represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even to Nematoda, they are thus referred as the “core” IntFam-241 group.
Mentions: To compare the intestinal transcriptomes of A. suum, H. contortus, and C. elegans in a single analysis, we built protein families from the complete set of 9,918 translated intestinal genes combined from the three nematodes. A total of 5,587 intestinal protein families (IntFam) were identified conservatively based on sequence similarities by MCL clustering [31] (Figure 4). Proteins assigned into the same protein family contain putative homologous or orthologous matches among the three species. Both diversification and conservation of the intestinal transcriptomes was obvious at the protein family level in this 3-species comparison. A total of 59% of all the sampled intestinal genes were members of the protein families containing proteins from only one nematode (Figure 4). Although the assignments for many of these single-species families are likely to change when more complete intestinal gene repertories become available, this group includes the genes contributing to the unique intestinal features in each species. The remaining 41% of the intestinal genes formed 910 multi-species protein families; they are conserved in the intestine of at least two nematodes. Among these multi-species families, 241 had members from all three species, accounting for ∼20% of all the intestinal genes under investigation (Figure 4). Given the differences in life styles and feeding patterns among the three nematodes, we propose that these 241 intestinal protein families represent an ancestral intestinal transcriptome involved in core cellular and physiological intestinal functions common to the investigated species or even across the Nematoda. Therefore, we referred to them as the “core” IntFam-241 group.

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