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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 : 000A54 ( Pmc/Curation ); précédent : 000A53; suivant : 000A55

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

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

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Robert A. Walker
<affiliation>
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<wicri:noCountry code="subfield">QLD 4878 Australia</wicri:noCountry>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland</nlm:aff>
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Philippa A. Sharman
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<wicri:noCountry code="subfield">QLD 4878 Australia</wicri:noCountry>
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Catherine M. Miller
<affiliation>
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<wicri:noCountry code="subfield">QLD 4878 Australia</wicri:noCountry>
</affiliation>
Nicholas C. Smith
<affiliation>
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<wicri:noCountry code="subfield">QLD 4878 Australia</wicri:noCountry>
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<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>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">BMC Genomics</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id>
<journal-title-group>
<journal-title>BMC Genomics</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2164</issn>
<publisher>
<publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25765081</article-id>
<article-id pub-id-type="pmc">4345034</article-id>
<article-id pub-id-type="publisher-id">1298</article-id>
<article-id pub-id-type="doi">10.1186/s12864-015-1298-6</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>RNA Seq analysis of the
<italic>Eimeria tenella</italic>
gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Walker</surname>
<given-names>Robert A</given-names>
</name>
<address>
<email>robert.walker1@jcu.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sharman</surname>
<given-names>Philippa A</given-names>
</name>
<address>
<email>philippasharman@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Miller</surname>
<given-names>Catherine M</given-names>
</name>
<address>
<email>kate.miller1@jcu.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lippuner</surname>
<given-names>Christoph</given-names>
</name>
<address>
<email>christoph.lippuner@dkf.unibe.ch</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
<xref ref-type="aff" rid="Aff4"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Okoniewski</surname>
<given-names>Michal</given-names>
</name>
<address>
<email>michal.okoniewski@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff5"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Eichenberger</surname>
<given-names>Ramon M</given-names>
</name>
<address>
<email>ramon.eichenberger@uzh.ch</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ramakrishnan</surname>
<given-names>Chandra</given-names>
</name>
<address>
<email>chandra.ramakrishnan@uzh.ch</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brossier</surname>
<given-names>Fabien</given-names>
</name>
<address>
<email>nicholas.smith@jcu.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff6"></xref>
<xref ref-type="aff" rid="Aff7"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Deplazes</surname>
<given-names>Peter</given-names>
</name>
<address>
<email>deplazesp@access.uzh.ch</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hehl</surname>
<given-names>Adrian B</given-names>
</name>
<address>
<email>adrian.hehl@uzh.ch</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Smith</surname>
<given-names>Nicholas C</given-names>
</name>
<address>
<email>nicholas.smith@jcu.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<aff id="Aff1">
<label></label>
Queensland Tropical Health Alliance Research Laboratory, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns Campus, McGregor Road, Smithfield, QLD 4878 Australia</aff>
<aff id="Aff2">
<label></label>
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland</aff>
<aff id="Aff3">
<label></label>
College of Public Health, Medical and Veterinary Sciences, James Cook University, Cairns Campus, McGregor Road, Smithfield, QLD 4878 Australia</aff>
<aff id="Aff4">
<label></label>
Department of Farm Animal, University of Zurich, Winterthurerstrasse, CH-8057 Zürich, Switzerland</aff>
<aff id="Aff5">
<label></label>
Functional Genomics Center Zurich, Winterthurerstrasse, CH-8057 Zürich, Switzerland</aff>
<aff id="Aff6">
<label></label>
Apicomplexes et Immunité Mucosale, INRA, UMR1282, Infectiologie et Santé Publique, F-37380 Nouzilly, France</aff>
<aff id="Aff7">
<label></label>
Université François Rabelais de Tours, UMR1282, Infectiologie et Santé Publique, F-37000 Tours, France</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>18</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>18</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>16</volume>
<issue>1</issue>
<elocation-id>94</elocation-id>
<history>
<date date-type="received">
<day>18</day>
<month>9</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>29</day>
<month>1</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>© Walker et al.; licensee BioMed Central. 2015</copyright-statement>
<license license-type="open-access">
<license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">http://creativecommons.org/licenses/by/4.0</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<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>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>
<italic>Eimeria tenella</italic>
</kwd>
<kwd>RNA Seq</kwd>
<kwd>Microgametocyte</kwd>
<kwd>Macrogametocyte</kwd>
<kwd>Oocyst</kwd>
<kwd>Fertilisation</kwd>
<kwd>Transmission</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2015</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>

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