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

Sequence Similarities Identified in the A. suum and H. contortus Intestinal Transcriptomes.The three phylogenetically specific sequence groups used to identify sequence similarities of the intestinal genes were: i) Caenorhabditis spp., amino acid sequences from the complete genomes of C. elegans, C. briggsae, and C. remanei, ii) Other Nematoda, non-Caenorhabditis nematode nucleic acid sequences excluding those from either A. suum or H. contortus, when sequences from A. suum or H. contortus were queried, respectively, and iii) Non-Nematoda, non-nematode amino acid sequences from the non-redundant protein database NR. In total, 61% (1,893/3,121) A. suum and 81% (1,423/1,755) H. contortus intestinal genes contained primary sequence similarities to known proteins from other organisms.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2483350&req=5

pntd-0000269-g001: Sequence Similarities Identified in the A. suum and H. contortus Intestinal Transcriptomes.The three phylogenetically specific sequence groups used to identify sequence similarities of the intestinal genes were: i) Caenorhabditis spp., amino acid sequences from the complete genomes of C. elegans, C. briggsae, and C. remanei, ii) Other Nematoda, non-Caenorhabditis nematode nucleic acid sequences excluding those from either A. suum or H. contortus, when sequences from A. suum or H. contortus were queried, respectively, and iii) Non-Nematoda, non-nematode amino acid sequences from the non-redundant protein database NR. In total, 61% (1,893/3,121) A. suum and 81% (1,423/1,755) H. contortus intestinal genes contained primary sequence similarities to known proteins from other organisms.

Mentions: Differences in the intestinal gene repertoires were obvious among the three nematodes. In total, 39% of A. suum and 19% of H. contortus intestinal genes were found to be novel compared to all known proteins in the public databases (Figure 1). Such novel intestine-expressed parasite genes contained no match in the complete genome of the free-living C. elegans, thus not in the C. elegans intestine, making them unique by comparison to C. elegans. In addition, for the sampled intestinal genes from both parasites, the non-Caenorhabditis nematodes offered the largest numbers of homologous matches than either the Caenorhabditis species or the non-nematode organisms (Figure 1). Such differences may suggest the existence of lineage- or species-specific diversification in the nematode intestine.


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)

Sequence Similarities Identified in the A. suum and H. contortus Intestinal Transcriptomes.The three phylogenetically specific sequence groups used to identify sequence similarities of the intestinal genes were: i) Caenorhabditis spp., amino acid sequences from the complete genomes of C. elegans, C. briggsae, and C. remanei, ii) Other Nematoda, non-Caenorhabditis nematode nucleic acid sequences excluding those from either A. suum or H. contortus, when sequences from A. suum or H. contortus were queried, respectively, and iii) Non-Nematoda, non-nematode amino acid sequences from the non-redundant protein database NR. In total, 61% (1,893/3,121) A. suum and 81% (1,423/1,755) H. contortus intestinal genes contained primary sequence similarities to known proteins from other organisms.
© Copyright Policy
Related In: Results  -  Collection

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

pntd-0000269-g001: Sequence Similarities Identified in the A. suum and H. contortus Intestinal Transcriptomes.The three phylogenetically specific sequence groups used to identify sequence similarities of the intestinal genes were: i) Caenorhabditis spp., amino acid sequences from the complete genomes of C. elegans, C. briggsae, and C. remanei, ii) Other Nematoda, non-Caenorhabditis nematode nucleic acid sequences excluding those from either A. suum or H. contortus, when sequences from A. suum or H. contortus were queried, respectively, and iii) Non-Nematoda, non-nematode amino acid sequences from the non-redundant protein database NR. In total, 61% (1,893/3,121) A. suum and 81% (1,423/1,755) H. contortus intestinal genes contained primary sequence similarities to known proteins from other organisms.
Mentions: Differences in the intestinal gene repertoires were obvious among the three nematodes. In total, 39% of A. suum and 19% of H. contortus intestinal genes were found to be novel compared to all known proteins in the public databases (Figure 1). Such novel intestine-expressed parasite genes contained no match in the complete genome of the free-living C. elegans, thus not in the C. elegans intestine, making them unique by comparison to C. elegans. In addition, for the sampled intestinal genes from both parasites, the non-Caenorhabditis nematodes offered the largest numbers of homologous matches than either the Caenorhabditis species or the non-nematode organisms (Figure 1). Such differences may suggest the existence of lineage- or species-specific diversification in the nematode intestine.

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