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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

Orthologous Genes Tend to Maintain Their Intestinal Expression Patterns across A. suum and C. elegans.A total of 289 putative orthologous pairs were identified among the intestine or gonad gene groups from A. suum and C. elegans. Ninety such pairs were found between the two intestine gene groups, representing an enrichment of 31% over the expectation from a random distribution of orthologous pairs, and an enrichment of only 5% was detected between genes in the two gonad groups. The  hypothesis of random orthologous pairing was rejected at a confidence level of at least 99% with a χ2 value of 11.9 between the observations and expectations.
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pntd-0000269-g003: Orthologous Genes Tend to Maintain Their Intestinal Expression Patterns across A. suum and C. elegans.A total of 289 putative orthologous pairs were identified among the intestine or gonad gene groups from A. suum and C. elegans. Ninety such pairs were found between the two intestine gene groups, representing an enrichment of 31% over the expectation from a random distribution of orthologous pairs, and an enrichment of only 5% was detected between genes in the two gonad groups. The hypothesis of random orthologous pairing was rejected at a confidence level of at least 99% with a χ2 value of 11.9 between the observations and expectations.

Mentions: To increase the confidence of analysis, we next focused on the putative orthologous pairs predicted among the intestine and gonad gene groups, which was a smaller data set than the homologous pairs used above but with higher stringency. Among the total of 1,652 putative orthologous pairs predicted from A. suum and C. elegans (see Materials and Methods), 289 were paired among genes from the intestine and gonad groups. They were used in a Chi Square statistical test, with random distribution of orthologous pairs as the hypothesis. Compared to the expected numbers, there was a 31% enrichment of orthologous pairs observed between the A. suum and C. elegans intestine groups (Figure 3), whereas the enrichment between the two gonad groups was only marginal (5%), and the observed numbers of orthologous pairs between the gonad and intestine groups were less than expected (Figure 3). Overall, a significant χ2 value of 11.9 rejects the hypothesis at a confidence level higher than 99% (p-value <0.01) [43], and selective pressure is evident on molecular conservation of the intestinal gene repertories.


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)

Orthologous Genes Tend to Maintain Their Intestinal Expression Patterns across A. suum and C. elegans.A total of 289 putative orthologous pairs were identified among the intestine or gonad gene groups from A. suum and C. elegans. Ninety such pairs were found between the two intestine gene groups, representing an enrichment of 31% over the expectation from a random distribution of orthologous pairs, and an enrichment of only 5% was detected between genes in the two gonad groups. The  hypothesis of random orthologous pairing was rejected at a confidence level of at least 99% with a χ2 value of 11.9 between the observations and expectations.
© Copyright Policy
Related In: Results  -  Collection

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

pntd-0000269-g003: Orthologous Genes Tend to Maintain Their Intestinal Expression Patterns across A. suum and C. elegans.A total of 289 putative orthologous pairs were identified among the intestine or gonad gene groups from A. suum and C. elegans. Ninety such pairs were found between the two intestine gene groups, representing an enrichment of 31% over the expectation from a random distribution of orthologous pairs, and an enrichment of only 5% was detected between genes in the two gonad groups. The hypothesis of random orthologous pairing was rejected at a confidence level of at least 99% with a χ2 value of 11.9 between the observations and expectations.
Mentions: To increase the confidence of analysis, we next focused on the putative orthologous pairs predicted among the intestine and gonad gene groups, which was a smaller data set than the homologous pairs used above but with higher stringency. Among the total of 1,652 putative orthologous pairs predicted from A. suum and C. elegans (see Materials and Methods), 289 were paired among genes from the intestine and gonad groups. They were used in a Chi Square statistical test, with random distribution of orthologous pairs as the hypothesis. Compared to the expected numbers, there was a 31% enrichment of orthologous pairs observed between the A. suum and C. elegans intestine groups (Figure 3), whereas the enrichment between the two gonad groups was only marginal (5%), and the observed numbers of orthologous pairs between the gonad and intestine groups were less than expected (Figure 3). Overall, a significant χ2 value of 11.9 rejects the hypothesis at a confidence level higher than 99% (p-value <0.01) [43], and selective pressure is evident on molecular conservation of the intestinal gene repertories.

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