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Mechanism and Field Potential Against Hylobius Abietis Larvae

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Mechanism and Field Potential Against Hylobius Abietis Larvae Interactions of entomopathogenic fungi and other control agents: mechanism and field potential against Hylobius abietis larvae A thesis submitted to the National University of Ireland, Maynooth for the degree of Doctor of Philosophy by Louise Mc Namara B.Sc. Supervisor Co-Supervisor Head of Department Dr. Christine Griffin Dr. Kevin Kavanagh Dr. Paul Moynagh Behavioural Ecology & Biocontrol Medical Mycology Unit Dept. of Biology Dept. of Biology Dept. of Biology Maynooth University Maynooth University Maynooth University County Kildare County Kildare County Kildare May 2016 DECLARATION This thesis has not been submitted in whole or part to this or any other university for any degree, and is the original work of the author except where otherwise stated. Signed: ______________ Date: ______________ II Acknowledgements I would like to firstly thank my supervisors, Dr. Christine Griffin and Dr. Kevin Kavanagh, for all their support and guidance throughout my PhD. I was very lucky to have two incredibly supportive supervisors, who were so generous with their time and help, and I am extremely grateful to have had the opportunity to work in both your research groups. Thank you to the Department of Agriculture, Food and the Marine, for funding my research project as part of the MCOP project, which was funded by the Irish government under the National Development Plan 2007-2013. I have had the opportunity to work with some many great people throughout my project. To Dr. James Carolan, thank you for your extensive help with proteomics and for helping me tackle Qexactive from the very start, I couldn’t even try to guess how many hours you spent helping me work through that data. Thank you to Dr. David Fitzpatrick and Dr. Sarah Connell for your assistance with my transcriptomic work. Thank you to Dr. Stephen Dolan for your extensive help with fungal analysis and metabolite identification. Thank you to Dr. Johan Stephens and Dr. John Walsh for your NMR work and metabolite identification. To Dr. Chris Williams thank you for teaching me everything I needed to know to do field trials. Thank you to Dr. Tolis Kapranas for all your help with statistics, particularly GenStat. Thank you to Padraig O’Tuama of Coillte for his assistance with providing field sites. To Prof. Martin Downes thank you for all your encouragement and very wise words over the years. And of course thank you to every field work assistant: in particular Ben, Lorna and Sarah Jane. To everyone in both my labs, past and present, thank you for making sure all this work still managed to be fun. I’m lucky to have made amazing friends during my PhD, especially Carla and Amie, Carla who I worked with from the very beginning and who made sure there was never a dull day, we even took on America and survived! Amie, you must be exhausted from listening to me while writing this thesis, but thanks for being such a great support and tea buddy! To Niall for teaching me everything I needed to know about Galleria. To Lorraine thanks for motivating me for the final stretch. Thanks to my other lab members: Ronan, Anatte, Fred, Gail, Johan, Cathryn, Mohammad and Julien for making Maynooth a great place to work. III Thank you to my family, my parents, Martin and Shirley, my brother Brian, my sister Carmel and Alfie, I would not be submitting this thesis if it wasn’t for your incredible support from the very beginning, thank you for always believing in me no matter what and for always helping me achieve my dreams. To Colm (and Tilly) thank for always making me laugh and destress throughout all my academic endeavours since our leaving cert days, I bet your glad it’s finally coming to an end! Lastly, to all the pine weevils and galleria who gave up their lives for this work: I literally couldn’t have done it without you! IV Abstract Biological control is the beneficial application of natural enemies such as pathogens, predators and parasites in managing pests and their damage. Entomopathogenic fungi (EPF) have a crucial role in natural ecosystems and are being developed as alternative control agents for insect pests. Both Beauvaria bassiana and Metarhizium anisopliae have been proven to be effective biological control agents against a range of pests and are commercially produced. Advantages of using EPF for biological pest control include their degree of specificity, absence of effects on mammals, reduced probability of insects developing resistance and they may persist for long periods in some environments which could provide long term control effects. Disadvantages include that it takes EPF longer to kill insects than their chemical counterparts, application needs to be timed for high relative humidity and low pest numbers, and efficacy varies among different insect species. If a combination of treatments resulted in a synergistic interaction then the efficacy of these biopesticides would be increased. A number of laboratory and field studies have used combinations of entomopathogenic nematodes (EPN) and EPF against insect pests with resulting interactions ranging from antagonistic to synergistic. In the case of synergism resulting from combined applications it is suggested that EPF may make the host more susceptible through suppressing its immune system. To understand how this putative synergistic interaction between control agents could occur mechanistically, the effect of EPF supernatant was tested on the immune response of the forestry pest, Hylobius abietis, to screen for species with immunomodulating properties. The potential of the commonly used model organism, the greater wax moth, Galleria mellonella, as a model for the study of the immune response of H. abietis to pathogens was also explored. Hylobius abietis, the large pine weevil, is a major pest of reforestation in Europe. It is estimated that H. abietis costs the forestry industry approximately €140 million/year. Current control measures rely heavily on the synthetic chemical cypermethrin. However, due to concerns over its environmental impact cypermethrin is being phased out across Europe. Therefore there is an interest in the use of entomopathogens as biological control agents in integrated pest management. Thus one objective of this work was to assess the efficacy of EPF, EPN and EPF-EPN V combinations for H. abietis suppression in the field in order to ultimately determine if the treatments used exert synergistic control over H. abietis. The effect of EPF supernatant on the immune response of insects was assessed through a number of bioassays that investigated the effect of EPF on haemocyte densities and yeast proliferation in the insect haemocoel, as well as testing whether pre-treatment with EPF increases larval susceptibility to subsequent pathogens. The effect of EPF supernatant on the humoral immune response was investigated by subjecting larval haemolymph to label free quantitative (LFQ) proteomic analysis. To enable proteomic investigations into the effects of EPF on the immune response of H. abietis and to compensate for the lack of genomic information for H. abietis; a de novo transcriptome study of H. abietis larvae was performed with Beijing Genomics Institute (BGI, Hong Kong). Bioassays indicated that M. anisopliae, B. bassiana and Beauveria caledonica, demonstrated immunomodulating effects on H. abietis larvae, while M. anisopliae and B. caledonica modulated the immune response of G. mellonella making the insect more susceptible to subsequent pathogens. LFQ analysis on larval haemolymph showed that in response to EPF supernatant both insect species displayed altered abundance of proteins involved in antimicrobial defence, the prophenoloxidase cascade, detoxification and detection and sensing. These patterns of alteration may be integral to the modulation of the host immune response by EPF. A major difference observed between the proteomic profiles of H. abietis and G. mellonella haemolymph was that H. abietis injected with B. caledonica supernatant had a major alteration in metabolic proteins involved in cellulose cleavage, reflective of its wood based diet. It was concluded G. mellonella may have an application as a model for looking for secondary metabolites or natural products that display immunomodulating properties so that EPF isolates could be screened for production of these products. However G. mellonella are not a substitute for the target pest for proteomic analysis. Moreover laboratory bioassays with either G. mellonella or H. abietis are not predictive of whether synergy will occur in the field as there are many more factors involved than just the ability of EPF to modulate the immune response. To investigate the ability of EPF and EPN to suppress H. abietis populations in the field, three field studies were carried out over three consecutive years. Treatments were applied to tree stumps harbouring H. abietis developmental stages. VI The efficacy of EPF and EPN was investigated alone and in combination through emergence trapping and destructive sampling. Three EPF strains were utilised in these field studies, commercial strains of M. anisopliae and B. bassiana and a strain of B. caledonica native to Ireland. Two EPN species were utilised in these field studies, Steinernema carpocapsae and Heterorhabditis downesi, the latter is native to Ireland. In this work EPN were found to offer superior control over H. abietis in the field than EPF, with all treatments that caused significant reduction in adult emergence being EPN alone or EPN in combination with EPF. Ultimately EPF are not suited to control of H. abietis using this strategy. Synergy between EPF-EPN was not achieved in any of the three field studies with all combinations tested giving additive results. The final aim of this work was to investigate if the little-studied native fungus B. caledonica produces immunomodulating compounds active against H. abietis. Identification, large scale production and structural determination of an abundant secreted natural product of B. caledonica was carried out using High Performance Liquid Chromatography (HPLC) and Nuclear magnetic resonance (NMR) spectroscopy, and the metabolite of interest was found to be oosporein.
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