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Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death

Jorge Luis Folch-Mallol, Tariq Butt Orcid Logo, Bethany P. J. Greenfield, Carolyn Greig, Thierry Maffeis Orcid Logo, James W. D. Taylor, Justyna Piasecka, Ed Dudley, Ahmed Abdulla, Ivan M. Dubovskiy, Inmaculada Garrido-Jurado, Enrique Quesada-Moraga, Mark W. Penny, Daniel C. Eastwood, Dan Eastwood Orcid Logo

PLoS ONE, Volume: 8, Issue: 12, Start page: e81686

Swansea University Authors: Tariq Butt Orcid Logo, Carolyn Greig, Thierry Maffeis Orcid Logo, Ed Dudley, Dan Eastwood Orcid Logo

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Abstract

Metarhizium anisopliae, a fungal pathogen of terrestrial arthropods, kills the aquatic larvae of Aedes aegypti, the vector of dengue and yellow fever. The fungus kills without adhering to the host cuticle. Ingested conidia also fail to germinate and are expelled in fecal pellets. This study investig...

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Published in: PLoS ONE
ISSN: 1932-6203
Published: 2013
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URI: https://cronfa.swan.ac.uk/Record/cronfa30740
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The fungus kills without adhering to the host cuticle. Ingested conidia also fail to germinate and are expelled in fecal pellets. This study investigates the mechanism by which this fungus adapted to terrestrial hosts kills aquatic mosquito larvae. Genes associated with the M. anisopliae early pathogenic response (proteinases Pr1 and Pr2, and adhesins, Mad1 and Mad2) are upregulated in the presence of larvae, but the established infection process observed in terrestrial hosts does not progress and insecticidal destruxins were not detected. Protease inhibitors reduce larval mortality indicating the importance of proteases in the host interaction. The Ae. aegypti immune response to M. anisopliae appears limited, whilst the oxidative stress response gene encoding for thiol peroxidase is upregulated. Cecropin and Hsp70 genes are downregulated as larval death occurs, and insect mortality appears to be linked to autolysis through caspase activity regulated by Hsp70 and inhibited, in infected larvae, by protease inhibitors. Evidence is presented that a traditional host-pathogen response does not occur as the species have not evolved to interact. M. anisopliae retains pre-formed pathogenic determinants which mediate host mortality, but unlike true aquatic fungal pathogens, does not recognise and colonise the larval host.</abstract><type>Journal Article</type><journal>PLoS ONE</journal><volume>8</volume><journalNumber>12</journalNumber><paginationStart>e81686</paginationStart><publisher/><issnElectronic>1932-6203</issnElectronic><keywords/><publishedDay>13</publishedDay><publishedMonth>12</publishedMonth><publishedYear>2013</publishedYear><publishedDate>2013-12-13</publishedDate><doi>10.1371/journal.pone.0081686</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2017-12-29T17:55:35.4248205</lastEdited><Created>2016-10-20T17:55:06.1877158</Created><path><level id="1">College of Science</level><level id="2">Biosciences</level></path><authors><author><firstname>Jorge Luis</firstname><surname>Folch-Mallol</surname><order>1</order></author><author><firstname>Tariq</firstname><surname>Butt</surname><orcid>0000-0002-8789-9543</orcid><order>2</order></author><author><firstname>Bethany P. 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spelling 2017-12-29T17:55:35.4248205 v2 30740 2016-10-20 Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death 85d1c2ddde272a1176e74978e25ebece 0000-0002-8789-9543 Tariq Butt Tariq Butt true false 7f95061328bd6726f7472ced9cb8d937 Carolyn Greig Carolyn Greig true false 992eb4cb18b61c0cd3da6e0215ac787c 0000-0003-2357-0092 Thierry Maffeis Thierry Maffeis true false c7d05f992a817cd3b9a5f946bd909b71 Ed Dudley Ed Dudley true false 4982f3fa83886c0362e2bb43ce1c027f 0000-0002-7015-0739 Dan Eastwood Dan Eastwood true false 2016-10-20 SBI Metarhizium anisopliae, a fungal pathogen of terrestrial arthropods, kills the aquatic larvae of Aedes aegypti, the vector of dengue and yellow fever. The fungus kills without adhering to the host cuticle. Ingested conidia also fail to germinate and are expelled in fecal pellets. This study investigates the mechanism by which this fungus adapted to terrestrial hosts kills aquatic mosquito larvae. Genes associated with the M. anisopliae early pathogenic response (proteinases Pr1 and Pr2, and adhesins, Mad1 and Mad2) are upregulated in the presence of larvae, but the established infection process observed in terrestrial hosts does not progress and insecticidal destruxins were not detected. Protease inhibitors reduce larval mortality indicating the importance of proteases in the host interaction. The Ae. aegypti immune response to M. anisopliae appears limited, whilst the oxidative stress response gene encoding for thiol peroxidase is upregulated. Cecropin and Hsp70 genes are downregulated as larval death occurs, and insect mortality appears to be linked to autolysis through caspase activity regulated by Hsp70 and inhibited, in infected larvae, by protease inhibitors. Evidence is presented that a traditional host-pathogen response does not occur as the species have not evolved to interact. M. anisopliae retains pre-formed pathogenic determinants which mediate host mortality, but unlike true aquatic fungal pathogens, does not recognise and colonise the larval host. Journal Article PLoS ONE 8 12 e81686 1932-6203 13 12 2013 2013-12-13 10.1371/journal.pone.0081686 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University 2017-12-29T17:55:35.4248205 2016-10-20T17:55:06.1877158 College of Science Biosciences Jorge Luis Folch-Mallol 1 Tariq Butt 0000-0002-8789-9543 2 Bethany P. J. Greenfield 3 Carolyn Greig 4 Thierry Maffeis 0000-0003-2357-0092 5 James W. D. Taylor 6 Justyna Piasecka 7 Ed Dudley 8 Ahmed Abdulla 9 Ivan M. Dubovskiy 10 Inmaculada Garrido-Jurado 11 Enrique Quesada-Moraga 12 Mark W. Penny 13 Daniel C. Eastwood 14 Dan Eastwood 0000-0002-7015-0739 15 0030740-02112017151812.pdf Buttetal2013MetarhiziumpathogenesisofAedeslarvae.pdf 2017-11-02T15:18:12.9600000 Output 2686262 application/pdf Version of Record true 2017-11-02T00:00:00.0000000 C 2013 Butt et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. true eng
title Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
spellingShingle Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
Tariq Butt
Carolyn Greig
Thierry Maffeis
Ed Dudley
Dan Eastwood
title_short Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
title_full Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
title_fullStr Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
title_full_unstemmed Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
title_sort Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death
author_id_str_mv 85d1c2ddde272a1176e74978e25ebece
7f95061328bd6726f7472ced9cb8d937
992eb4cb18b61c0cd3da6e0215ac787c
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author_id_fullname_str_mv 85d1c2ddde272a1176e74978e25ebece_***_Tariq Butt
7f95061328bd6726f7472ced9cb8d937_***_Carolyn Greig
992eb4cb18b61c0cd3da6e0215ac787c_***_Thierry Maffeis
c7d05f992a817cd3b9a5f946bd909b71_***_Ed Dudley
4982f3fa83886c0362e2bb43ce1c027f_***_Dan Eastwood
author Tariq Butt
Carolyn Greig
Thierry Maffeis
Ed Dudley
Dan Eastwood
author2 Jorge Luis Folch-Mallol
Tariq Butt
Bethany P. J. Greenfield
Carolyn Greig
Thierry Maffeis
James W. D. Taylor
Justyna Piasecka
Ed Dudley
Ahmed Abdulla
Ivan M. Dubovskiy
Inmaculada Garrido-Jurado
Enrique Quesada-Moraga
Mark W. Penny
Daniel C. Eastwood
Dan Eastwood
format Journal article
container_title PLoS ONE
container_volume 8
container_issue 12
container_start_page e81686
publishDate 2013
institution Swansea University
issn 1932-6203
doi_str_mv 10.1371/journal.pone.0081686
college_str College of Science
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hierarchy_top_title College of Science
hierarchy_parent_id collegeofscience
hierarchy_parent_title College of Science
department_str Biosciences{{{_:::_}}}College of Science{{{_:::_}}}Biosciences
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description Metarhizium anisopliae, a fungal pathogen of terrestrial arthropods, kills the aquatic larvae of Aedes aegypti, the vector of dengue and yellow fever. The fungus kills without adhering to the host cuticle. Ingested conidia also fail to germinate and are expelled in fecal pellets. This study investigates the mechanism by which this fungus adapted to terrestrial hosts kills aquatic mosquito larvae. Genes associated with the M. anisopliae early pathogenic response (proteinases Pr1 and Pr2, and adhesins, Mad1 and Mad2) are upregulated in the presence of larvae, but the established infection process observed in terrestrial hosts does not progress and insecticidal destruxins were not detected. Protease inhibitors reduce larval mortality indicating the importance of proteases in the host interaction. The Ae. aegypti immune response to M. anisopliae appears limited, whilst the oxidative stress response gene encoding for thiol peroxidase is upregulated. Cecropin and Hsp70 genes are downregulated as larval death occurs, and insect mortality appears to be linked to autolysis through caspase activity regulated by Hsp70 and inhibited, in infected larvae, by protease inhibitors. Evidence is presented that a traditional host-pathogen response does not occur as the species have not evolved to interact. M. anisopliae retains pre-formed pathogenic determinants which mediate host mortality, but unlike true aquatic fungal pathogens, does not recognise and colonise the larval host.
published_date 2013-12-13T03:52:09Z
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