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RNA Seq analysis of the Eimeria tenella gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis

Identifieur interne : 002931 ( Main/Exploration ); précédent : 002930; suivant : 002932

RNA Seq analysis of the Eimeria tenella gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis

Auteurs : Robert A. Walker [Suisse] ; Philippa A. Sharman ; Catherine M. Miller ; Christoph Lippuner [Suisse] ; Michal Okoniewski [Suisse] ; Ramon M. Eichenberger [Suisse] ; Chandra Ramakrishnan [Suisse] ; Fabien Brossier [France] ; Peter Deplazes [Suisse] ; Adrian B. Hehl [Suisse] ; Nicholas C. Smith

Source :

RBID : PMC:4345034

Descripteurs français

English descriptors

Abstract

Background

The protozoan Eimeria tenella is a common parasite of chickens, causing avian coccidiosis, a disease of on-going concern to agricultural industries. The high prevalence of E. tenella can be attributed to the resilient oocyst stage, which is transmitted between hosts in the environment. As in related Coccidia, development of the eimerian oocyst appears to be dependent on completion of the parasite’s sexual cycle. RNA Seq transcriptome profiling offers insights into the mechanisms governing the biology of E. tenella sexual stages (gametocytes) and the potential to identify targets for blocking parasite transmission.

Results

Comparisons between the sequenced transcriptomes of E. tenella gametocytes and two asexual developmental stages, merozoites and sporozoites, revealed upregulated gametocyte transcription of 863 genes. Many of these genes code for proteins involved in coccidian sexual biology, such as oocyst wall biosynthesis and fertilisation, and some of these were characterised in more depth. Thus, macrogametocyte-specific expression and localisation was confirmed for two proteins destined for incorporation into the oocyst wall, as well as for a subtilisin protease and an oxidoreductase. Homologues of an oocyst wall protein and oxidoreductase were found in the related coccidian, Toxoplasma gondii, and shown to be macrogametocyte-specific. In addition, a microgametocyte gamete fusion protein, EtHAP2, was discovered.

Conclusions

The need for novel vaccine candidates capable of controlling coccidiosis is rising and this panel of gametocyte targets represents an invaluable resource for development of future strategies to interrupt parasite transmission, not just in Eimeria but in other Coccidia, including Toxoplasma, where transmission blocking is a relatively unexplored strategy.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1298-6) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-015-1298-6
PubMed: 25765081
PubMed Central: 4345034


Affiliations:


Links toward previous steps (curation, corpus...)


Le document en format XML

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<term>Amino Acid Sequence</term>
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<term>Chickens (parasitology)</term>
<term>Coccidiosis (parasitology)</term>
<term>Coccidiosis (pathology)</term>
<term>Eimeria tenella (genetics)</term>
<term>Eimeria tenella (growth & development)</term>
<term>Genome, Protozoan</term>
<term>Merozoites (metabolism)</term>
<term>Microscopy, Fluorescence</term>
<term>Molecular Sequence Data</term>
<term>Oocysts (metabolism)</term>
<term>Oxidoreductases (genetics)</term>
<term>Oxidoreductases (metabolism)</term>
<term>Protozoan Proteins (genetics)</term>
<term>Protozoan Proteins (metabolism)</term>
<term>RNA (chemistry)</term>
<term>RNA (isolation & purification)</term>
<term>Recombinant Proteins (biosynthesis)</term>
<term>Recombinant Proteins (chemistry)</term>
<term>Recombinant Proteins (genetics)</term>
<term>Sequence Alignment</term>
<term>Sequence Analysis, RNA</term>
<term>Sporozoites (metabolism)</term>
<term>Transcriptome</term>
</keywords>
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<term>ARN ()</term>
<term>ARN (isolement et purification)</term>
<term>Alignement de séquences</term>
<term>Analyse de séquence d'ARN</term>
<term>Animaux</term>
<term>Coccidiose (anatomopathologie)</term>
<term>Coccidiose (parasitologie)</term>
<term>Données de séquences moléculaires</term>
<term>Eimeria tenella (croissance et développement)</term>
<term>Eimeria tenella (génétique)</term>
<term>Génome de protozoaire</term>
<term>Microscopie de fluorescence</term>
<term>Mérozoïtes (métabolisme)</term>
<term>Oocystes (métabolisme)</term>
<term>Oxidoreductases (génétique)</term>
<term>Oxidoreductases (métabolisme)</term>
<term>Poulets (parasitologie)</term>
<term>Protéines de protozoaire (génétique)</term>
<term>Protéines de protozoaire (métabolisme)</term>
<term>Protéines recombinantes ()</term>
<term>Protéines recombinantes (biosynthèse)</term>
<term>Protéines recombinantes (génétique)</term>
<term>Sporozoïtes (métabolisme)</term>
<term>Séquence d'acides aminés</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en">
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>RNA</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Oxidoreductases</term>
<term>Protozoan Proteins</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr">
<term>Coccidiose</term>
</keywords>
<keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr">
<term>Protéines recombinantes</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Eimeria tenella</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Eimeria tenella</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Eimeria tenella</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Eimeria tenella</term>
<term>Oxidoreductases</term>
<term>Protéines de protozoaire</term>
<term>Protéines recombinantes</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="isolation & purification" xml:lang="en">
<term>RNA</term>
</keywords>
<keywords scheme="MESH" qualifier="isolement et purification" xml:lang="fr">
<term>ARN</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Merozoites</term>
<term>Oocysts</term>
<term>Oxidoreductases</term>
<term>Protozoan Proteins</term>
<term>Sporozoites</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Mérozoïtes</term>
<term>Oocystes</term>
<term>Oxidoreductases</term>
<term>Protéines de protozoaire</term>
<term>Sporozoïtes</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitologie" xml:lang="fr">
<term>Coccidiose</term>
<term>Poulets</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitology" xml:lang="en">
<term>Chickens</term>
<term>Coccidiosis</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en">
<term>Coccidiosis</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Amino Acid Sequence</term>
<term>Animals</term>
<term>Genome, Protozoan</term>
<term>Microscopy, Fluorescence</term>
<term>Molecular Sequence Data</term>
<term>Sequence Alignment</term>
<term>Sequence Analysis, RNA</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>ARN</term>
<term>Alignement de séquences</term>
<term>Analyse de séquence d'ARN</term>
<term>Animaux</term>
<term>Données de séquences moléculaires</term>
<term>Génome de protozoaire</term>
<term>Microscopie de fluorescence</term>
<term>Protéines recombinantes</term>
<term>Séquence d'acides aminés</term>
<term>Transcriptome</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>The protozoan
<italic>Eimeria tenella</italic>
is a common parasite of chickens, causing avian coccidiosis, a disease of on-going concern to agricultural industries. The high prevalence of
<italic>E. tenella</italic>
can be attributed to the resilient oocyst stage, which is transmitted between hosts in the environment. As in related Coccidia, development of the eimerian oocyst appears to be dependent on completion of the parasite’s sexual cycle. RNA Seq transcriptome profiling offers insights into the mechanisms governing the biology of
<italic>E. tenella</italic>
sexual stages (gametocytes) and the potential to identify targets for blocking parasite transmission.</p>
</sec>
<sec>
<title>Results</title>
<p>Comparisons between the sequenced transcriptomes of
<italic>E. tenella</italic>
gametocytes and two asexual developmental stages, merozoites and sporozoites, revealed upregulated gametocyte transcription of 863 genes. Many of these genes code for proteins involved in coccidian sexual biology, such as oocyst wall biosynthesis and fertilisation, and some of these were characterised in more depth. Thus, macrogametocyte-specific expression and localisation was confirmed for two proteins destined for incorporation into the oocyst wall, as well as for a subtilisin protease and an oxidoreductase. Homologues of an oocyst wall protein and oxidoreductase were found in the related coccidian,
<italic>Toxoplasma gondii</italic>
, and shown to be macrogametocyte-specific. In addition, a microgametocyte gamete fusion protein, EtHAP2, was discovered.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>The need for novel vaccine candidates capable of controlling coccidiosis is rising and this panel of gametocyte targets represents an invaluable resource for development of future strategies to interrupt parasite transmission, not just in
<italic>Eimeria</italic>
but in other Coccidia, including
<italic>Toxoplasma</italic>
, where transmission blocking is a relatively unexplored strategy.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-015-1298-6) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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