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Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control

Esam Hummadi, Alex Dearden, Tom Generalovic, Benjamin Clunie, Alexandria Harrott, Yarkin Cetin, Merve Demirbek, Salim Khoja Orcid Logo, Dan Eastwood Orcid Logo, Ed Dudley, Selcuk Hazir, Mustapha Touray, Derya Ulug, Sebnem Hazal Gulsen, Harun Cimen, Tariq Butt Orcid Logo

Biological Control, Volume: 155, Start page: 104527

Swansea University Authors: Esam Hummadi, Alex Dearden, Tom Generalovic, Benjamin Clunie, Yarkin Cetin, Merve Demirbek, Salim Khoja Orcid Logo, Dan Eastwood Orcid Logo, Ed Dudley, Tariq Butt Orcid Logo

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DOI (Published version): 10.1016/j.biocontrol.2020.104527

Abstract

The entomopathogenic fungus (EPF) Metarhizium brunneum occupies the same ecological niche as entomopathogenic nematodes (EPN), with both competing for insects as a food source in the rhizosphere. Interactions between these biocontrol agents can be antagonistic or synergistic. To better understand th...

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Published in: Biological Control
ISSN: 1049-9644
Published: Elsevier BV 2021
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Interactions between these biocontrol agents can be antagonistic or synergistic. To better understand these interactions, this study focussed on investigating the effect of M. brunneum volatile organic compounds (VOCs), 1-octen-3-ol and 3-octanone, on EPN survival and behaviour. These VOCs proved to be highly toxic to the infective juveniles (IJs) of the EPN Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora with mortality being dose dependent. Chemotaxis studies of H. bacteriophora IJs in Pluronic F127 gel revealed significant preference for the VOCs compared with controls for all tested concentrations. The VOCs also impacted on the test insects in a dose-dependent manner with 3-octanone being more toxic to Galleria mellonella, Cydia splendana and Curculio elephas larvae than 1-octen-3-ol. Mortality of C. splendana and G. mellonella larvae was significantly higher when exposed to relatively high doses (&gt;25%) of 3-octanone. Lower doses of 3-octanone and 1-octen-3-ol immobilised test insects, which recovered after exposure to fresh air for 2 hrs. In depth studies on H. bacteriophora showed that exposure of IJs to &gt; 10% concentration of 3-octanone or 1-octen-3-ol negatively affected infectivity whereas exposure to lower doses (0.1%, 0.01%) had no effect. The VOCs affected IJs, reducing penetration efficacy and the number of generations inside G. mellonella but they failed to inhibit the bacterial symbiont, Photorhabdus kayaii. The ecological significance of VOCs and how they could influence EPF-EPN insect interactions is discussed.</abstract><type>Journal Article</type><journal>Biological Control</journal><volume>155</volume><journalNumber/><paginationStart>104527</paginationStart><paginationEnd/><publisher>Elsevier BV</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>1049-9644</issnPrint><issnElectronic/><keywords>Metarhizium brunneumen, tomopathogenic nematodes, volatile organic compounds, nematicide, semiochemicals</keywords><publishedDay>1</publishedDay><publishedMonth>4</publishedMonth><publishedYear>2021</publishedYear><publishedDate>2021-04-01</publishedDate><doi>10.1016/j.biocontrol.2020.104527</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm/><funders>UKRI, BB/L012472/1</funders><lastEdited>2021-02-11T12:14:55.6355541</lastEdited><Created>2020-12-30T12:33:47.8179938</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Biosciences, Geography and Physics - Biosciences</level></path><authors><author><firstname>Esam</firstname><surname>Hummadi</surname><order>1</order></author><author><firstname>Alex</firstname><surname>Dearden</surname><order>2</order></author><author><firstname>Tom</firstname><surname>Generalovic</surname><order>3</order></author><author><firstname>Benjamin</firstname><surname>Clunie</surname><order>4</order></author><author><firstname>Alexandria</firstname><surname>Harrott</surname><order>5</order></author><author><firstname>Yarkin</firstname><surname>Cetin</surname><order>6</order></author><author><firstname>Merve</firstname><surname>Demirbek</surname><order>7</order></author><author><firstname>Salim</firstname><surname>Khoja</surname><orcid>0000-0003-3763-6769</orcid><order>8</order></author><author><firstname>Dan</firstname><surname>Eastwood</surname><orcid>0000-0002-7015-0739</orcid><order>9</order></author><author><firstname>Ed</firstname><surname>Dudley</surname><order>10</order></author><author><firstname>Selcuk</firstname><surname>Hazir</surname><order>11</order></author><author><firstname>Mustapha</firstname><surname>Touray</surname><order>12</order></author><author><firstname>Derya</firstname><surname>Ulug</surname><order>13</order></author><author><firstname>Sebnem Hazal</firstname><surname>Gulsen</surname><order>14</order></author><author><firstname>Harun</firstname><surname>Cimen</surname><order>15</order></author><author><firstname>Tariq</firstname><surname>Butt</surname><orcid>0000-0002-8789-9543</orcid><order>16</order></author></authors><documents><document><filename>55947__19074__adeb464c48f04e409ff6322e86211661.pdf</filename><originalFilename>55947).pdf</originalFilename><uploaded>2021-01-15T14:37:03.6501780</uploaded><type>Output</type><contentLength>2881548</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; 2020 The Author(s). 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spelling 2021-02-11T12:14:55.6355541 v2 55947 2020-12-30 Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control 1c141b261d5c2534b3c2fadb94e90e75 Esam Hummadi Esam Hummadi true false 4386276ca8a14b9b73fbcb9e69ea1527 Alex Dearden Alex Dearden true false 8b8d4daaade7c9f8bf2d72c5090508b5 Tom Generalovic Tom Generalovic true false cce29e902d62a050c29943d30fbe9455 Benjamin Clunie Benjamin Clunie true false 93dcb1e0bae52051387a45ac092cc257 Yarkin Cetin Yarkin Cetin true false 91419a7a254ab4affd7e58b239dc4f31 Merve Demirbek Merve Demirbek true false 7b244b69ad0a81fc0cabd6b8ae7e9f1f 0000-0003-3763-6769 Salim Khoja Salim Khoja true false 4982f3fa83886c0362e2bb43ce1c027f 0000-0002-7015-0739 Dan Eastwood Dan Eastwood true false c7d05f992a817cd3b9a5f946bd909b71 Ed Dudley Ed Dudley true false 85d1c2ddde272a1176e74978e25ebece 0000-0002-8789-9543 Tariq Butt Tariq Butt true false 2020-12-30 SBI The entomopathogenic fungus (EPF) Metarhizium brunneum occupies the same ecological niche as entomopathogenic nematodes (EPN), with both competing for insects as a food source in the rhizosphere. Interactions between these biocontrol agents can be antagonistic or synergistic. To better understand these interactions, this study focussed on investigating the effect of M. brunneum volatile organic compounds (VOCs), 1-octen-3-ol and 3-octanone, on EPN survival and behaviour. These VOCs proved to be highly toxic to the infective juveniles (IJs) of the EPN Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora with mortality being dose dependent. Chemotaxis studies of H. bacteriophora IJs in Pluronic F127 gel revealed significant preference for the VOCs compared with controls for all tested concentrations. The VOCs also impacted on the test insects in a dose-dependent manner with 3-octanone being more toxic to Galleria mellonella, Cydia splendana and Curculio elephas larvae than 1-octen-3-ol. Mortality of C. splendana and G. mellonella larvae was significantly higher when exposed to relatively high doses (>25%) of 3-octanone. Lower doses of 3-octanone and 1-octen-3-ol immobilised test insects, which recovered after exposure to fresh air for 2 hrs. In depth studies on H. bacteriophora showed that exposure of IJs to > 10% concentration of 3-octanone or 1-octen-3-ol negatively affected infectivity whereas exposure to lower doses (0.1%, 0.01%) had no effect. The VOCs affected IJs, reducing penetration efficacy and the number of generations inside G. mellonella but they failed to inhibit the bacterial symbiont, Photorhabdus kayaii. The ecological significance of VOCs and how they could influence EPF-EPN insect interactions is discussed. Journal Article Biological Control 155 104527 Elsevier BV 1049-9644 Metarhizium brunneumen, tomopathogenic nematodes, volatile organic compounds, nematicide, semiochemicals 1 4 2021 2021-04-01 10.1016/j.biocontrol.2020.104527 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University UKRI, BB/L012472/1 2021-02-11T12:14:55.6355541 2020-12-30T12:33:47.8179938 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Esam Hummadi 1 Alex Dearden 2 Tom Generalovic 3 Benjamin Clunie 4 Alexandria Harrott 5 Yarkin Cetin 6 Merve Demirbek 7 Salim Khoja 0000-0003-3763-6769 8 Dan Eastwood 0000-0002-7015-0739 9 Ed Dudley 10 Selcuk Hazir 11 Mustapha Touray 12 Derya Ulug 13 Sebnem Hazal Gulsen 14 Harun Cimen 15 Tariq Butt 0000-0002-8789-9543 16 55947__19074__adeb464c48f04e409ff6322e86211661.pdf 55947).pdf 2021-01-15T14:37:03.6501780 Output 2881548 application/pdf Version of Record true © 2020 The Author(s). This is an open access article under the CC BY license true eng http://creativecommons.org/licenses/by/4.0/
title Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
spellingShingle Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
Esam Hummadi
Alex Dearden
Tom Generalovic
Benjamin Clunie
Yarkin Cetin
Merve Demirbek
Salim Khoja
Dan Eastwood
Ed Dudley
Tariq Butt
title_short Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
title_full Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
title_fullStr Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
title_full_unstemmed Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
title_sort Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control
author_id_str_mv 1c141b261d5c2534b3c2fadb94e90e75
4386276ca8a14b9b73fbcb9e69ea1527
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93dcb1e0bae52051387a45ac092cc257
91419a7a254ab4affd7e58b239dc4f31
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author_id_fullname_str_mv 1c141b261d5c2534b3c2fadb94e90e75_***_Esam Hummadi
4386276ca8a14b9b73fbcb9e69ea1527_***_Alex Dearden
8b8d4daaade7c9f8bf2d72c5090508b5_***_Tom Generalovic
cce29e902d62a050c29943d30fbe9455_***_Benjamin Clunie
93dcb1e0bae52051387a45ac092cc257_***_Yarkin Cetin
91419a7a254ab4affd7e58b239dc4f31_***_Merve Demirbek
7b244b69ad0a81fc0cabd6b8ae7e9f1f_***_Salim Khoja
4982f3fa83886c0362e2bb43ce1c027f_***_Dan Eastwood
c7d05f992a817cd3b9a5f946bd909b71_***_Ed Dudley
85d1c2ddde272a1176e74978e25ebece_***_Tariq Butt
author Esam Hummadi
Alex Dearden
Tom Generalovic
Benjamin Clunie
Yarkin Cetin
Merve Demirbek
Salim Khoja
Dan Eastwood
Ed Dudley
Tariq Butt
author2 Esam Hummadi
Alex Dearden
Tom Generalovic
Benjamin Clunie
Alexandria Harrott
Yarkin Cetin
Merve Demirbek
Salim Khoja
Dan Eastwood
Ed Dudley
Selcuk Hazir
Mustapha Touray
Derya Ulug
Sebnem Hazal Gulsen
Harun Cimen
Tariq Butt
format Journal article
container_title Biological Control
container_volume 155
container_start_page 104527
publishDate 2021
institution Swansea University
issn 1049-9644
doi_str_mv 10.1016/j.biocontrol.2020.104527
publisher Elsevier BV
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description The entomopathogenic fungus (EPF) Metarhizium brunneum occupies the same ecological niche as entomopathogenic nematodes (EPN), with both competing for insects as a food source in the rhizosphere. Interactions between these biocontrol agents can be antagonistic or synergistic. To better understand these interactions, this study focussed on investigating the effect of M. brunneum volatile organic compounds (VOCs), 1-octen-3-ol and 3-octanone, on EPN survival and behaviour. These VOCs proved to be highly toxic to the infective juveniles (IJs) of the EPN Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora with mortality being dose dependent. Chemotaxis studies of H. bacteriophora IJs in Pluronic F127 gel revealed significant preference for the VOCs compared with controls for all tested concentrations. The VOCs also impacted on the test insects in a dose-dependent manner with 3-octanone being more toxic to Galleria mellonella, Cydia splendana and Curculio elephas larvae than 1-octen-3-ol. Mortality of C. splendana and G. mellonella larvae was significantly higher when exposed to relatively high doses (>25%) of 3-octanone. Lower doses of 3-octanone and 1-octen-3-ol immobilised test insects, which recovered after exposure to fresh air for 2 hrs. In depth studies on H. bacteriophora showed that exposure of IJs to > 10% concentration of 3-octanone or 1-octen-3-ol negatively affected infectivity whereas exposure to lower doses (0.1%, 0.01%) had no effect. The VOCs affected IJs, reducing penetration efficacy and the number of generations inside G. mellonella but they failed to inhibit the bacterial symbiont, Photorhabdus kayaii. The ecological significance of VOCs and how they could influence EPF-EPN insect interactions is discussed.
published_date 2021-04-01T04:10:32Z
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score 11.037253

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