Progress 01/01/12 to 12/30/12
Outputs
OUTPUTS: Research: (I) Exploiting and improving mycoinsecticides. Research and experiments were conducted in (a) the molecular mechanisms pathogenesis using the entomopathogenic fungus, Beauveria bassiana and its insects as a model system and (b)developing novel approaches to improve the utility and use of microbial agents for insect control. Research in the lab focuses on characterizing molecular and biochemical pathways of the fungus. Outputs include increased knowledge concerning: (1) fungal proteins involved in insect epicuticle interactions and degradation and (2) novel approaches in which critical insect biochemical pathways can be subverted for pest control purposes. (II) Functional genomics and genetics of insect pathogenic fungi. The laboratory has developed novel protocols for genetic modfication of fungi that does not use antibiotic selective markers and has developed a sequence and genomics base for examining gene expression during B. bassiana growth, development, and infection of insects. Genes have been identified and characterized from the B. bassiana genome involved as virulence factors, regulators of virulence, and as novel insect toxins. Educational: We have developed instructional materials for use in K-12 classrooms introducing fungi and insects to students. PARTICIPANTS: PI/PD Dr. Nemat O. Keyhani, designed experiments, interpreted results, wrote manuscripts, participated in dissemination of results (conferences and meetings). Dr. Zhibing Luo, designed, executed, and interpreted experiments, edited manuscripts, participated in dissemination of results (conferences and meetings). Dr. Yuqi Qin, designed, executed, and interpreted experiments, edited manuscripts, participated in dissemination of results (conferences and meetings). Dr. Almudena Ortiz, designed, executed, and interpreted experiments, edited manuscripts, participated in dissemination of results (conferences and meetings). Arun Wanchoo (graduate student) designed, executed, and interpreted experiments. Training and Development: The research opportunities afforded by the project have been integrated with a training and development program at all levels of instruction including high-school (summer internship), undergraduate, graduate, and post-doctoral levels. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The research impacts insect control and insect borne disease causing agent transmission, as well as fundamental ecological processes. (1) Insect control. We have demonstrated that insect molecules can be used against the insects themselves using entomopathogenic fungi as a vehicle for the delivery of these molecules to the insects. This idea was validated against the yellow fever mosquito, Aedes aegyptii and against the red imported fire ant, Solenopsis invicta. (2) Fundamental ecological processes. We have used B. bassiana and their insect hosts as a model system for the genetic dissection of host-pathogen evolution and interactions by characterizing (a) signal transduction pathways in the fungus responsive to host cues, (b)a set of related enzymes, termed cytochrome P450s, implicated in hydrocabon assimilation pathways, proteins potentially critical for the ability of the fungus to penetrate the insect cuticle, and (c) novel toxins and secondary metabolites generated by the fungus under different growth conditions.
Publications
- Keyhani, N.O. (2012) Using host molecules to increase fungal virulence for biological control of insects. Virulence 3(4): 415-418.
- Zhang, S., Widemann, E., Bernard. G, Lesot, A., Pinot, F., Pedrini, N., and Keyhani, N.O. (2012) CYP52X1, representing a new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in the entomopathogenic fungus Beauveria bassiana. J. Biol. Chem. 287: 13477-13486.
- Fan, Y., Borovsky, D., Hawkings, C., Ortiz-Urquiza, A., and Keyhani, N.O. (2012) Exploiting host molecules to augment mycoinsecticide virulence. Nature Biotechnol. 30: 35-37
- Fan, Y., Pereira, R.M., Kilic, E., Casella, G., and Keyhani, N.O. (2012) Pyrokinin β-neuropeptide affects necrophoretic behavior in fire ants, and expression of β-NP in a mycoinsecticide increases its virulence. PLoS One 7(1): e26924.
- Luo, X, Keyhani, N.O., Yu, X., He, Z., Luo, Z., Pei, Y., and Zhang, Y. (2012) The MAP kinase Bbslt2 controls growth conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genet. Biol. 49: 544-555
- Fan, Y., Ortiz-Urquiza, A., Kudia, R., and Keyhani, N.O. (2012) Bbcsa1, a fungal homolog of neuronal calcium sensor-1 regulates extracellular acidification and contributes to virulence in the entomopathogenic fungus Beauveria bassiana. Microbiology, 158: 1843-1851.
- Mantilla, J.G., Galeano, N.F., Gaitan, A.L., Christancho, M.A., Keyhani, N.O. and Gongora, C.E. (2012) Comparative transcriptome analysis of the entomopathogenic fungus Beauveria bassiana grown on the coffee berry borer (Hypothenemus hampei). Microbiology, 158: 1826-1842.
- Glare, T., Caradus, J., Gelernter, W., Jackson, T., Keyhani, N., Kohl, J., Marrone, P., Morin, L., and Stewart, A. Have biopesticides come of age (2012) Trends in Biotechnology 30: 250-258.
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Progress 10/01/10 to 09/30/11
Outputs
OUTPUTS: Activities: Research: The laboratory has several broad interrelated projects that center around the entomopathogenic fungus Beauveria bassiana and its interactions with insect hosts. Research and experiments were conducted in the following major areas. Molecular mechanisms of fungal pathogenesis: The laboratory examines the virulence of the entomopathogenic fungus, Beauveria bassiana towards insects as a model system. Research in the lab focuses on characterizing the molecular and biochemical characteristics of the enzymes, inducers, and regulators of fungal attachment and infection of insects. Despite interaction with the insect (epi)-cuticle being the first step in pathogensis, little is known about the fungal determinants and signaling pathways that respond to cuticular cues. Outputs include increased knowledge concerning: (1) the pathways for insect epicuticle attachment and alkane and insect waxy layer degradation by (a) construction and characterization of targeted genomic knockouts of candidate genes involved in epicuticle sensing and/or degradation and (b) analysis of cuticle degrading enzyme activities in B. bassiana, and (2) functional genomics, we have determined the functions of some genes both induced and non-induced during the infection process. Approaches used in the lab range from molecular biology to biochemistry and cell biology. Genetics of fungal mediated insect-biocontrol: The laboratory has developed a sequence and genomics base for examining gene expression during B. bassiana growth, development, and infection of insects. Projects involve mining of the B. bassiana genome for novel enzyme activities and virulence regulators. A deep transcriptome sequencing effort has recently been completed (unpublished) that has examined fungal responses to cuticular hydrocarbons. Aside from genes whose functions could be assigned, we identified an interesting subset of genes unknown function that are highly expressed when the fungus was grown on specific insect cuticular components. Several projects revolve around deciphering the roles of these genes via bioiformatic predictions and genetic approaches. Products: Based upon our research a provisional patent has been submitted by the University of Florida as follows: Fan, Y and Keyhani, N.O. Exploiting host molecules to augment the virulence of mycoinsecticides. University of Florida, Provisional Patent Application, Oct 2011. PARTICIPANTS: PI/PD Dr. Nemat O. Keyhani, designed experiments, interpreted results, wrote manuscripts, participated in dissemination of results (conferences and meetings). Dr. Sheng-hua Ying, designed, executed, and interpreted experiments, edited manuscripts, participated in dissemination of results (conferences and meetings). Dr. Yanhua Fan, designed, executed, and interpreted experiments, edited manuscripts, participated in dissemination of results (conferences and meetings). Dr. Engin Kilic, executed and interpreted experiments. Arun Wanchoo (graduate student) designed, executed, and interpreted experiments. Training and Development: The research opportunities afforded by the project have been integrated with a training and development program at all levels of instruction including high-school (summer internship), undergraduate, graduate, and post-doctoral levels. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The research impacts fundamental ecological processes that includes host-pathogen interactions, eukaryotic evolution, maintenance of C/N cycles and biodiversity, novel enzymatic transformations, and biological control of insect pests. (1) Maintenance of C and N cycles. Insect bodies account for a significant amount of biomass and terrestrial ecosystems would be severely depleted in C and N in a matter of decades and the respective cycles would cease if these bodies were not converted to biologically useful form. Significant components of insect cuticles are insoluble polymers and hydrocarbons, and cuticle assimilating organisms such as B. bassiana play an important role in the remediation and turnover of these compounds. Our research has identified novel enzymes involved in the turnover of insect cuticular lipids. (2) Pathogen evolution. Entomopathogenic fungi offer an under-exploited source of inference regarding disease processes and the evolution of pathogens. The diversity of target organisms coupled to the ancient nature of the host-pathogen interaction renders these organisms as excellent model systems for examining the origins and mechanisms underlying pathogenesis. We have begun to delineate the pathways for epicuticle degradation and perform comparative analyses with other pathogens (i.e. plant pathogenic fungi). This work is aimed towards addressing one of the major issues concerning the lifestyle and evolution of these fungi, namely what makes these fungi entomopathogens, distinguishing them from saprophytes, and plant and animal pathogens. Given that the closest fungal relatives of B. bassiana include plant epiphytes, endophytes (B. bassiana itself can exists as an endophyte of certain plants) and pathogens, our research has yielded important insights into the mechanisms and evolution of host switching (from plants to insects) which we hypothesize involves both adaptations of biochemical pathways for plant cuticle penetration to insect cuticle penetration as well as the evolution of novel fungal-insect pathogen specific pathways. (3) Improved biopesticides. As an alternative to chemical pesticides and compatible with organic farming practices, B. bassiana is an EPA approved commercially available biological control agent for a variety of insect pests. Understanding the genes and their protein products important for virulence or able to degrade specific hydrocarbon constituents, can lead to rational design strategies for strain improvement, including the better targeting of specific insects. We have begun to use our insights for strain improvement, Use of fungi represents a sustainable and renewable system, and our research has additional important implications for examining effects of climate change on insects and their fungal predators.
Publications
- Keyhani, N.O. (2011) Fungal genomes and beyond. Fungal Genom. Biol. 1:1e101
- Zhang, S., Xia, Y., Kim, B., and Keyhani, N.O. (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development, and pathogenesis in the entomopathogenic fungus Beauveria bassiana, Mol. Micobiol. 80: 811-826
- Zhang, S., Xia, Y., and Keyhani, N.O. (2011) Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative GPI-anchored β-glucanosyltransferase to conidial thermotolerance and virulence. Appl. Environ. Microbiol. 77: 2676-2684
- Fan, Y., Zhang, S., Kruer-Zerhusen, N., and Keyhani, N.O. (2011) High-throughput insertion mutagenesis and screening of clones of the entomopathogenic fungus Beauveria bassiana. J. Invert. Pathology 106: 274-279
- Kirkland, B.H. and Keyhani, N.O. (2011) Expression and purification of a functionally active Class I fungal hydrophobin from the entomopathogenic fungus Beauveria bassiana in E. coli. J. Indust. Micro. & Biotech. 38: 327-335
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Progress 10/01/05 to 09/30/11
Outputs
Target Audience: Target audiences have included (1) high school, undergraduate, gradaute, and Postdoctoral students, and (2) professional scientists . Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? Research skills that have been developed by participants in the project include training in molecular biology, biochemistry, and cell biology. Specific training has included learning molecular genetics and manipulation of fungi, protein expression and enzyme characterization, and microscopy, the latter ranging from light and fluorescence to electron microscopy. Notable specific training includes: For the Postdoctoral Fellow- gaining of expertise in construction of targeted gene-knockouts in fungi, establishing genetic screens, and construction of expression libraries. For the graduate student- expertise has been acquired in cell biology, protein expression, purification, and characterization, and insect pathology For the undergraduate-Undergraduates have contributed to all aspects of the project including in screening of gene-knockout transformants, protein expression and purification and the microscopy. Two students have gained significant experience in electron microscopy and one student has successfully completed an Honor Thesis which has include extensive microscopic analyses and has led to the student being a coauthor on a paper that has been submitted. Teaching The Postdoctoral fellow is involved in the development of lectures dealing with fungal insect interactions and insect pathology. All students in the lab participate in weekly lab meetings and journal article discussions. How have the results been disseminated to communities of interest? Results have been published in peer-reviewed journals including Molecular Microbiology, Applied and Environmental Microbiology, Microbiology, Journal of Invertebrate Pathology, and Fungal Genomics. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
This research project deals with deciphering the molecular mechanisms that underlying the interactions between an insect fungal pathogen, Beauveria bassiana, and their target hosts. Fungal pathogens of insects represent vital natural regulators of insect populations in many ecosystems and these organisms are currently being developed and used as alternatives to chemical pesticides for insect control. The project seeks to understand the biochemical and genetic underpinnings of how the fungus breaches the insect waxy layer, the first and most important protective defense mechanism insect use to thwart microbial pathogens. Notable experimental activities in this reporting period include: Experiments were performed regarding the biochemical and genetic characterization of fungal spore proteins, termed hydrophobins, involved in attachment to insect hosts. The roles of two hydrophobins were probed via genetic and biochemcial approaches. Based upon previous results, we hypothesized that hydrophobins could be exploited for application as novel surface modifying agents to potentially build cell scaffolds and antimicrobial substrata. Experiments were performed to develop a robust methods for expression and purification of the hydrophobin proteins. A high-throughput genetic screening approach and contruction of a random mutant library was developed for B. bassiana in order to isolate pathogenicity related genes. The relationship between cell wall structural epitopes and spore thermotolerence and virulence was examined via characterization of a glycosyltransferase in B. bassiana.
Publications
- Type:
Journal Articles
Status:
Accepted
Year Published:
2011
Citation:
Zhang, S., Xia, Y., Kim, B., and Keyhani, N.O. (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development, and pathogenesis in the entomopathogenic fungus Beauveria bassiana, Mol. Micobiol. 80: 811-826
- Type:
Journal Articles
Status:
Accepted
Year Published:
2011
Citation:
Zhang, S., Xia, Y., and Keyhani, N.O. (2011) Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative GPI-anchored ?-glucanosyltransferase to conidial thermotolerance and virulence. Appl. Environ. Microbiol. 77: 2676-2684
- Type:
Journal Articles
Status:
Accepted
Year Published:
2011
Citation:
Fan, Y., Zhang, S., Kruer-Zerhusen, N., and Keyhani, N.O. (2011) High-throughput insertion mutagenesis and screening of clones of the entomopathogenic fungus Beauveria bassiana. J. Invert. Pathology 106: 274-279
- Type:
Journal Articles
Status:
Accepted
Year Published:
2011
Citation:
Kirkland, B.H. and Keyhani, N.O. (2011) Expression and purification of a functionally active Class I fungal hydrophobin from the entomopathogenic fungus Beauveria bassiana in E. coli. J. Indust. Micro. & Biotech. 38: 327-335
- Type:
Journal Articles
Status:
Accepted
Year Published:
2011
Citation:
Keyhani, N.O. (2011) Fungal genomes and beyond. Fungal Genom. Biol. 1:1e101
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Progress 10/01/09 to 09/30/10
Outputs
OUTPUTS: Research activities conducted in the reporting period impact the maintenance of C and N cycles, pathogen evolution, surface signaling and fungal spore coat structure, enzymatic transformations, and improvement of biologically based pesticides. As an alternative to chemical pesticides and compatible with organic farming practices, B. bassiana is an EPA approved commercially available biological control agent for a variety of insect pests. This project seeks to understand the genes and their protein products important for virulence or able to degrade specific hydrocarbon constituents, which can lead to rational design strategies for strain improvement, including the better targeting of specific insects. Major outputs in the reporting period include molecular isolation of a set of cytochrome p450 enzymes implicated in insect hydrocarbon degradation by entomopathogenic fungi, an exploration of the evolution and maintenance of insect virulence by these essentially soil-dwelling organisms, and the development of molecular methods for the genetic engineering of entomopathogenic fungi. PARTICIPANTS: PI: Nemat O. Keyhani, formultated the experimental plan, mentored students and Postdocs in the lab, disseminated outcomes via writing of peer-reviewed manuscripts. No USDA-CREES funding for reporting period. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
(1) Little is known concerning the enzymes and pathways responsible for degrading the insect epicuticle and its hydrocarbon constituents by entomopathogenic fungi such as B. bassiana. Eight cytochrome p450 enzymes were isolated from B. bassiana, including members of novel p450 families and subfamilies. Expression studies suggest a role for these enzymes in in host hydrocarbon assimilation, and potentially as targets whose overexpression may increase fungal virulence towards insect pests. Critical in this regards are observations that chemically resistant insects continue to be susceptible to entomopathogenic fungi. (2)The insect immune system, particularly phagocytic heamocytes, is analogous to the mammalian macrophage. Findings from the lab suggest that entomopathogenic fungi are able to evade insect immune systems and that this ability may be a consequence of adaptations that have evolved in order to aviod predation by soil amoebae. These data may help explain the persistence of virulence in these essentially soil/arborial dwelling fungi, that are capable of saprophytic growth but which have evolved mechanisms of targeted insects. (3) The laboratory has also developed robust techniques for the molecular manipulation of B. bassiana. These methods are likely to allow for greater genetic dissection of the pathways that mediate insect virulence and development of entomopathogenic fungi, in particular B. bassiana.
Publications
- Pedrini, N., Zhang, S., Juarez, M.P., Keyhani, N.O. (2010) Molecular characterization and expression analysis of a suite of cytochrome P450 enzymes implicated in insect hydrocarbon degradation in the entomopathogenic fungus Beauveria bassiana. Microbiology 156: 2549-2557
- Zhang, S., Fan, Y., Xia, Y. X., and Keyhani, N.O. (2010) Sulfonylurea resistance as a new selectable marker for the entomopathogenic fungus Beauveria bassiana. Appl Microbiol and Biotech 87:1151-1156
- Bidochka, M.J., Clark, D.C., Lewis, M.W., and Keyhani, N.O. (2010) Could insect phagocytic avoidance by entomogenous fungi have evolved via selection against soil amoeboid predators Microbiology 156:2164-2171
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Progress 10/01/08 to 09/30/09
Outputs
OUTPUTS: Fungal-insect interactions have profound implications in environmental microbiology, ecosystem balance, biodiversity, eukaryotic and pathogen evolution, and insect & pest control issues. The broad host range entomopathogenic fungus, Beauveria bassiana and their arthropod hosts have been engaged in a continuous struggle in relation to pathogen tactics designed to overcome ever changing host defenses. In this porject, we have examined the interaction of the fungus with the insect waxy layer as this is the first step in pathogenesis. We have begun to deipher the biochemical nature and genetic mechanisms that underlie insect waxy layer degradation by B. bassiana towards the goal of rational design strategies for improving the efficacy and safety of these organisms as part of Integrated Pest Management Practices. Using homology based searches of transcript libraries constructed in the lab, we have identified a set of genes involved in host epicuticle hydrocarbon degradation. Forward and reverse genetic approaches are being used to identify additional genes involved in these processes. Targeted gene-knockouts of candidate genes are being coupled to the biochemical characterization of enzymes important in the degradation of insect waxy layer constituents. In the process, we are determining the substrate specificities and kinetics of a set of cytochrome P450 enzymes, which include members of novel P450 families and subfamilies that we have identified and hypothesize to be specifically involved in waxy layer degradation. The characterization of genes and their protein products are being linked to their roles in the biology of the organism particularly with respect to development and pathogenesis. Whereas some of the genes we have identified are conserved amongst other fungi (and beyond), given the co-evolution of the predator-prey interaction between the fungus and target insect hosts, unique and novel biochemical pathways are also being characterized that have evolved in the fungus to degrade and overcome the insect epicuticle layer. We have published our results from the previsou year in three peer reviewed publications. PARTICIPANTS: PI: Nemat O. Keyhani, formultated the experimental plan, mentored students and Postdocs in the lab, disseminated outcomes via writing of peer-reviewed manuscripts. No members of the lab recieved USDA-CSREES funding (FY2009). TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Research derived from this proposal impacts fundamental ecological processes that includes host-pathogen interactions, eukaryotic evolution, maintenance of C/N cycles and biodiversity, novel enzymatic transformations, and biological control of insect pests. (1) Maintenance of C and N cycles. Insect bodies account for a significant amount of biomass and terrestrial ecosystems would be severely depleted in C and N in a matter of decades and the respective cycles would cease if these bodies were not converted to biologically useful form. Significant components of insect cuticles are insoluble polymers and hydrocarbons, and cuticle assimilating organisms such as B. bassiana play an important role in the remediation and turnover of these compounds. (2) Pathogen evolution. Entomopathogenic fungi offer an under-exploited source of inference regarding disease processes and the evolution of pathogens. The diversity of target organisms coupled to the ancient nature of the host-pathogen interaction renders these organisms as excellent model systems for examining the origins and mechanisms underlying pathogenesis. By delineating the pathways for epicuticle degradation this project seeks to address one of the major issues concerning the lifestyle and evolution of these fungi, namely what makes these fungi entomopathogens, distinguishing them from saprophytes, and plant and animal pathogens. Given that the closest fungal relatives of B. bassiana include plant epiphytes, endophytes (B. bassiana itself can exists as an endophyte of certain plants) and pathogens, research from this proposal is likely to yield important insights into the mechanisms and evolution of host switching (from plants to insects) which we hypothesize involves both adaptations of biochemical pathways for plant cuticle penetration to insect cuticle penetration as well as the evolution of novel fungal-insect pathogen specific pathways. (3) Enzymatic transformations. Aliphatic hydrocarbons represent a class of compounds with tremendous pharmaceutical and biotechnological applications; however, the C-C and C-H bonds in these molecules are inert to most organic transformation. The suite of cytochrome P450 enzymes under examination in this project, which include novel members of P450 families and subfamilies, are able to precisely perform such reactions, i.e. install oxygen into the aliphatic C-H bonds of these compounds, reactions that remain elusive to chemical approaches. Thus, studies on the substrate specificities and kinetics of these enzymes may lead to new biotechnological transformations and applications. (4) Improved biopesticides. As an alternative to chemical pesticides and compatible with organic farming practices, B. bassiana is an EPA approved commercially available biological control agent for a variety of insect pests. Understanding the genes and their protein products important for virulence or able to degrade specific hydrocarbon constituents, can lead to rational design strategies for strain improvement, including the better targeting of specific insects.
Publications
- de Crecy, E., Jaronski, S., Lyons, B., Lyons, T.J., and Keyhani, N.O. (2009) Directed evolution of a filamentous fungus for thermotolerance, BMC Biotechnology, 9:74
- Lewis, M.W., Robalino, I.V., and Keyhani, N.O. (2009) Uptake of the fluorescent probe FM4-64 by hyphae and hemolymph-derived in vivo hyphal bodies of the entomopathogenic fungus Beauveria bassiana, Microbiology, 155: 3110-3120
- Wanchoo, A., Lewis, M.W., and Keyhani, N.O. (2009) Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and hemolymph derived cells of the entomopathogenic fungus Beauveria bassiana, Microbiology, 155: 3121-3133.
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Progress 10/01/07 to 09/30/08
Outputs
OUTPUTS: Our goals are to investigate the biochemical and genetic determinants of the entomopathogenic fungus Beauveria bassiana during the infection and degradation of its insect host. Knowledge gained from this research can be expected to lead to rational design efforts for improving strain efficacy and utility. Experimental activities have included establishment of phage based screening for surface bioactive molecules dervied from the fungus, an examination of the surface properties of the fungus, and establishment of an in vitro insect cell culture based system for examining host-pathogen interactions. PARTICIPANTS: Dr. Nemat O. Keyhani (PI) TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
The findings and results derived from the research have led to the characterization of a groups of unqie fungal proteins termed hydrophobins, with the potential for novel biotechnological applications. This research is actively being pursued in the lab.
Publications
- Kurtti, T. and Keyhani, N.O. (2008) Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae, Microbiology 154: 1700-1709
- Holder, D.H, Kirkland, B.H., Michael W. Lewis, and Keyhani, N.O. (2007) Surface characteristics of the entomopathogenic fungus Beauveria (Cordyceps) bassiana, Microbiology 153: 3448-3457
- Cho, Eun-Min, Kirkland, B.H., Holder, D.H. and Keyhani, N.O. (2007) Phage display cDNA cloning and expression analysis of hydrophobins from the entomopathogenic fungus Beauveria (Cordyceps) bassiana, Microbiology 153: 3438-3447
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