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Introduction
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July 1999 - present
Publications
Publications (240)
Fungi are central to every terrestrial and many aquatic ecosystems, but the mechanisms underlying fungal tolerance to mercury, a global pollutant, remain unknown. Here, we show that the plant symbiotic fungus Metarhizium robertsii degrades methylmercury and reduces divalent mercury, decreasing mercury accumulation in plants and greatly increasing t...
Metarhizium spp. mediate multiple interactions that are usually positive with respect to their long-term plant environment, and negative with respect to short-lived hosts. In particular, their ability to kill a wide range of insects maximizes protection to the plants and provides a resource of nitrogen that the fungus trades with the plant for carb...
Ingenious exploitation of transgenic approaches to produce malaria resistant or sterile mosquitoes, or hypervirulent mosquito pathogens, has produced many potential solutions to vector borne diseases. However, in spite of technological feasibility, it has not been determined how well these new methods will work, and how they should be tested and re...
The complex nature of climate change-mediated multitrophic interaction is an underexplored area, but has the potential to dramatically shift transmission and distribution of many insects and their pathogens, placing some populations closer to the brink of extinction. However, for individual insect-pathogen interactions climate change will have comp...
The genus Metarhizium and Pochonia chlamydosporia comprise a monophyletic clade of highly abundant globally distributed fungi that can transition between long-term beneficial associations with plants to transitory pathogenic associations with frequently encountered protozoans, nematodes or insects. Some very common ‘specialist generalist’ species a...
We found substantial variation in resistance to the fly-specific pathogen Entomophthora muscae 'Berkeley' (Entomophthoromycota), in 20 lines from the Drosophila melanogaster Genetic Reference Panel (DGRP). Resistance to E. muscae is positively (r = 0.55) correlated with resistance to the broad host range ascomycete entomopathogen Metarhizium anisop...
A diverse set of pathogens have evolved extended phenotypes that manipulate the moribund behavior of their various insect hosts. By elevating host positioning at death, a phenomenon called “summit disease”, these pathogens have been shown to have higher fitness. Though a few summit disease systems have been intensively characterized, in particular...
Targeting mosquitoes to target malaria
Anopheline mosquitoes transmit the malaria parasite, but the insects themselves are prone to their own infections. Lovett et al. engineered a specific fungal pathogen of anophelines to carry insect-selective toxins. The effectiveness of this fungus for controlling mosquitoes was trialed in near-field condition...
Significance
Recently emerged fungal diseases are contributing toward global declines in wildlife, but the mechanisms for emergence of new pathogenic fungi remain mysterious. The entomopathogen Metarhizium robertsii evolved from plant symbionts, and here we report that this host shift was facilitated by 18 horizontal gene transfers (HGTs). The nece...
The major fungal phyla have independently and repeatedly evolved the ability to overcome the insect defense system, which is usually highly effective against fungal attack. During the genomic era of the last decade, extensive progress has been made in understanding the mechanisms of interactions between insects and their fungal pathogens, particula...
In Africa, adult mosquito populations are primarily controlled with insecticide‐impregnated bed nets and residual insecticide sprays. This coupled with widespread applications of pesticides in agriculture has led to increasing insecticide resistance in mosquito populations. We have developed multiple alternative strategies for exploiting transgenic...
Transgenic Metarhizium pingshaense expressing the spider neurotoxin Hybrid (Met-Hybrid) kill mosquitoes faster and at lower spore doses than wild-type strains. In this study, we demonstrate that this approach dovetails with the cornerstone of current malaria control: pyrethroid-insecticides, which are the cornerstone of current malaria control. We...
The assembly of irritability cone tests to study the impact of fungal infection on the flight capacity of mosquitoes.
(TIFF)
Results of World Health Organization (WHO) susceptibility tests of the impact of fungal infection on insecticide-susceptibility of wild caught mosquitoes from Burkina Faso and laboratory Anopheles gambiae Kisumu strain.
(DOCX)
Supplemental R codes of analysis.
(PDF)
Mortality percentage of mosquitoes over 24 h and a week observation after 1 h exposure in WHO cylinder to insecticides and fungi.
(DOCX)
Schematic of hybrid activity on an insect neuron.
(TIFF)
Background:
Genetically enhanced Metarhizium pingshaense are being developed for malaria vector control in Burkina Faso. However, not much is known about the local prevalence and pathogenicity of this fungus, so we prospected mosquitoes and plant roots (a common habitat for Metarhizium spp.) for entomopathogenic fungi.
Results:
Our investigation...
It is commonly observed that microorganisms subjected to a mild stress develop tolerance not only to higher doses of the same stress, but also to other stresses—a phenomenon called cross protection. The mechanisms for cross protection have not been fully revealed. Here we report that heat shock induced cross protection against UV, oxidative and osm...
Metarhizium robertsii is a versatile fungus with saprophytic, plant symbiotic and insect pathogenic lifestyle options. Here we show that M. robertsii mediates the saprophyte-to-insect pathogen transition through modulation of the expression of a membrane protein, Mr-OPY2. Abundant Mr-OPY2 protein initiates appressorium formation, a prerequisite for...
Heat tolerance is well known to be key to fungal survival in many habitats, but our mechanistic understanding of how organisms adapt to heat stress is still incomplete. Using Metarhizium robertsii , an emerging model organism for assessing evolutionary processes, we report that pyruvate is in the vanguard of molecules that scavenge heat-induced rea...
The plant root colonizing insect-pathogenic fungus Metarhizium robertsii has been shown to boost plant growth, but little is known about the responsible mechanisms. Here we show that M. robertsii promotes lateral root growth and root hair development of Arabidopsis seedlings in part through an auxin [indole-3-acetic acid (IAA)]-dependent mechanism....
The continued success of malaria control efforts requires the development, study and implementation of new technologies that circumvent insecticide resistance. We previously demonstrated that fungal pathogens can provide an effective delivery system for mosquitocidal or malariacidal biomolecules. Here we compared genes from arthropod predators enco...
Metarhizium robertsii occupies a wide array of ecological niches and has diverse lifestyle options (saprophyte, insect pathogen and plant symbiont), that renders it an unusually effective model for studying genetic mechanisms for fungal adaptation. Here we screened over 20,000 M. robertsii T-DNA mutants in order to elucidate genetic mechanism by wh...
Individuals vary extensively in the way they respond to disease but the genetic basis of this variation is not fully understood. We found substantial individual variation in resistance and tolerance to the fungal pathogen Metarhizium anisopliae Ma549 using the Drosophila melanogaster Genetic Reference Panel (DGRP). In addition, we found that host d...
Absolute rankings for fly lines for different phenotypic traits.
(XLSX)
Ma549 LT50 top association human orthologs
(XLSX)
Mean LT50 values for Ma549 and PA14, and Wolbachia infection status (WI).
(DOCX)
ANOVA table for Wolbachia and common inversions.
(XLSX)
Fungi are the commonest pathogens of insects and crucial regulators of insect populations. The rapid advance of genome technologies has revolutionized our understanding of entomopathogenic fungi with multiple Metarhizium spp. sequenced, as well as Beauveria bassiana, Cordyceps militaris, and Ophiocordyceps sinensis among others. Phylogenomic analys...
The study of infection and immunity in insects has achieved considerable prominence with the appreciation that their host defense mechanisms share many fundamental characteristics with the innate immune system of vertebrates. Studies on the highly tractable model organism Drosophila in particular have led to a detailed understanding of conserved in...
The two major aldehydes (E)-2-hexenal and (E)-2-octenal emitted as defensive secretions by bed bugs Cimex lectularius L. (Hemiptera: Cimicidae), inhibit the in vitro growth of an isolate of Metarhizium anisopliae sensu lato (s.l.) (Metsch.) Sokorin (Hypocreales: Clavicipitaceae) (ARSEF 1548). These chemicals inhibit fungal growth by direct contact...
Fungi cause the majority of insect disease. However, to date attempts to model host-fungal interactions with Drosophila have focused on opportunistic human pathogens. Here, we performed a screen of 2,613 mutant Drosophila lines to identify host genes affecting susceptibility to the natural insect pathogen Metarhizium anisopliae (Ma549). Overall, 24...
Locusts and grasshoppers (acridids) are among the worst pests of crops and grasslands worldwide. Metarhizium acridum, a fungal pathogen that specifically infects acridids, has been developed as a control agent but its utility is limited by slow kill time and greater expense than chemical insecticides. We found that expression of four insect specifi...
Bed bugs Cimex lectularius L. were exposed to conidia (spores) of the entomopathogenic fungus Metarhizium anisopliae by feeding, aerosol spray, or contact with a treated surface. Feeding experiments demonstrated that bed bugs were innately susceptible to this fungus. However, only at 98% humidity were mortality rates high, regardless of whether bed...
The brown marmorated stink bug (BMSB) is a highly destructive invasive pest that continues to be a source of damage in both food crop and ornamental systems. Recent efforts to evaluate entomopathogenic fungi such as Metarhizium anisopliae, Beauveria bassiana and Isaria fumosorosea for management of BMSB have proven largely ineffective. In an effort...
Significance
Fossil records have provided compelling evidence for evolution, but lack of existing transitional species has hindered our understanding of speciation at the molecular level. Genomic analyses of seven Metarhizium species revealed a directional speciation continuum from specialists with narrow host ranges to transitional species and the...
The insect pathogenic plant root symbiont Metarhizium experiences many situations that restrict its growth whether living in host insects or on plant roots. These include a range of physical, chemical and biological effects involving UV and extremes of temperature, pH, nutrient availability, toxic metals and other pollutants, and insect host defens...
Metarhizium species have recently been found to be plant rhizosphere associates as well as insect pathogens. Because of their abundance, rhizospheric Metarhizium could have enormous environmental impact, with co-evolutionary implications. Here, we tested the hypothesis that some Metarhizium spp. are multifactorial plant growth promoters. In two con...
Metarhizium robertsii is a plant root colonizing fungus that is also an insect pathogen. Its entomopathogenicity is a characteristic that was acquired during evolution from a plant endophyte ancestor. This transition provides a novel perspective on how new functional mechanisms important for host switching and virulence have evolved. From a random...
Significance
The ability of parasites to modify the behavior of their hosts is a widespread phenomenon, but the underlying mechanisms remain to be deciphered. Locusts such as Locusta migratoria manilensis are infamous for their ability to aggregate into gregarious migratory swarms that pose a major threat to food security. The microsporidian parasi...
Temperature extremes are an important adverse factor limiting the effectiveness of microbial pest control agents. They reduce virulence and persistence in the plant root-colonizing insect pathogen Metarhizium robertsii. Small heat shock proteins have been shown to confer thermotolerance in many organisms. In this study, we report on the cloning and...
Since tools of modern biotechnology have become available, the most commonly applied and often discussed genetically modified organisms are genetically modified crop plants, although genetic engineering is also being used successfully in organisms other than plants, including bacteria, fungi, insects, and viruses. Many of these organisms, as with c...
In response to fungal infection, the insect innate immune system produces a group of antimicrobial peptides. Drosomycin is Drosophila’s prevalent antifungal peptide and homologs are produced by diverse insects. Its production in response to fungal attack is mainly regulated by the Toll immune pathway. We used a Drosophila strain with a drosomycin-G...
As well as killing pest insects, the rhizosphere competent insect-pathogenic fungus Metarhizium robertsii also boosts plant growth by providing nitrogenous nutrients and increasing resistance to plant pathogens. Plant roots secrete abundant nutrients but little is known about their utilization by Metarhizium spp. and the mechanistic basis of Metarh...
Metarhizium anisopliae and Beauveria bassiana are both biological control agents approved by the US Environmental Protection Agency (EPA). Most research on fungal insect pathogens has focused on Beauveria and Metarhizium spp. They have a worldwide distribution from the arctic to the tropics and colonize an impressive array of environments including...
The caterpillar fungus Ophiocordyceps sinensis (best known as Cordyceps sinensis) mummifies ghost moth larvae exclusively in Tibetan Plateau alpine ecosystems. Touted as “Himalayan Viagra”, the fungus is highly prized due to its medical benefits and dwindling supplies. Attempts to culture the sexual fruiting-body have failed and the huge market dem...
Due in part to its documented agility at evolving resistance to currently available chemical insecticides, the bed bug Cimex lectularius has become increasingly difficult to control. Biopesticides such as the entomopathogenic fungus Metarhizium anisopliae are logical candidates for bed bug control since they are considered to be inherently safer th...
The low survival of microbial pest control agents exposed to UV is the major environmental factor limiting their effectiveness. Using gene disruption we demonstrated that the insect pathogenic fungus Metarhizium robertsii uses photolyases to remove UV-induced cyclobutane pyrimidine dimers (CPD) and pyrimidine (6-4) photoproducts [(6-4)PPs] from its...
The amount of CPDs in the solar-irradiated mycelium of wild type and transgenic B. bassiana expressing a CPD photolyase (HsPHR2) from H. salinarum. The quantification of CPDs was performed by ELISA with CPD monoclonal antibody. Blue: wild type; Orange: a transgenic strain expressing HsPHR2.
(PDF)
The sequences of primers and synthesized genes used in the study.
(PDF)
Phylogenetic analysis of photolyase domain (A) and FAD domain (B) of MrPHR1 and their homologs from bacterium, archae, insect and plant. MEGA5 software was used to carry out the analysis. Bootstrap values are adjacent to each internal node, representing the percentage of 1,000 bootstrap replicates.
(PDF)
Kinetics of mosquito survivorship in bioassays. Female adult mosquitoes (A. gambiae) were sprayed with B. bassiana spore suspensions (1×107 spores/mL) that were irradiated by sunlight for 4 h. Red = the wild type strain; Blue = a transgenic strain expressing a CPD photolyase (HsPHR2) from H. salinarum; black = control insects that were treated with...
The ability to repair CPDs of wild type and transgenic M. robertsii and B. bassiana radiated by UV followed by photoreactivation.
(PDF)
The ascomycete fungus Beauveria bassiana is a pathogen of hundreds of insect species and is commercially produced as an environmentally friendly mycoinsecticide. We sequenced the genome of B. bassiana and a phylogenomic analysis confirmed that ascomycete entomopathogenicity is polyphyletic, but also revealed convergent evolution to insect pathogeni...
Supplementary figures and tables
Phylogenetic analysis of MrCYP52 along with known fungal cytochrome P450 encoding genes. MEGA4 software was used to carry out the analysis. Bootstrap values are adjacent to each internal node, representing the percentage of 1,000 bootstrap replicates.
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Nucleotide sequence of the 5′-upstream region of the MrCYP52 gene. The translation start point is shown in bold. The putative CREA-binding sites are underlined.
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Primers used in this study.
(DOCX)
Disruption of MrCYP52 in M. robertsii using the Bar gene. (A) Strategy for targeted disruption of MrCYP52. Arrows indicate location of PCR primers. (B) Confirmation of the disruption of MrCYP52 by Southern blot analysis. 1: the wild type strain; 2: the MrCYP52 disruptant strain; 3: ΔMrCYP52 was complemented with the wild type MrCYP52; (C) Confirmat...
TMpred hydrophilicity analysis of
MrCYP52.
Shown is a plot of the
MrCYP52
amino acid numbers (X coordinate) against the probability that a specific amino acid is part (positive values on the y coordinate) or not part (negative values on the y coordinate) of a transmembrane helix. Solid and dotted lines indicated the probability of a putative tr...
Germination and appressorial formation (in brackets) against plastic or insect cuticle.
(DOCX)