The Multifaceted Beauveria bassiana and Other Insect-Related Fungi

A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Environmental and Ecological Interactions of Fungi".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 23525

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Guest Editor
Instituto de Investigaciones Bioquímicas de La Plata (INIBIOLP), National University of La Plata (UNLP), La Plata 1900, Argentina
Interests: entomopathogenic fungi; insect immunity; fungus–insect interaction; gene expression; fungal secondary metabolites; virulence factors
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Special Issue Information

Dear Colleagues,

Since Agostino Bassi isolated the fungal pathogenic agent of the white muscardine in insects (later named as Beauveria bassiana in his honor), and Élie Metchnikoff cultivated Metarhizium anisopliae as a first approach to use fungi as pest control agents, many other entomopathogenic fungi have been studied over the last two centuries. Fungus–insect interactions are known to drive pathogenic cycles that usually culminate in killing the hosts; however, these fungi are also facultative saprophytes in the soil and/or the rhizosphere. B. bassiana can also develop endophytic relationships with plants, conferring a level of protection to the host plant from the insects that feed on them. In addition to invertebrate pathology, B. bassiana also has diverse applications in a range of other disciplines, including as an important whole cell eukaryotic biocatalyst, and, together with other entomopathogenic fungi, remains a reservoir for the discovery of numerous secondary metabolites with bioactive functions.

This Special Issue will be focus on all aspects of the interaction between either B. bassiana or other insect-related fungi and their wide range of hosts, including arthropods and plants, as well as on the expression of secondary metabolites, such as toxins, antibiotics, anti-inflammatory and anti-proliferative molecules, plus other aspects regarding their catalyst role in biotransformation and bioremediation.

Dr. Nicolás Pedrini
Guest Editor

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Keywords

  • entomopathogenic fungi
  • fungi–host interaction
  • endophytic fungi
  • bioremediation
  • secondary metabolites

Published Papers (9 papers)

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Research

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20 pages, 4245 KiB  
Article
Contributions of a Histone Deacetylase (SirT2/Hst2) to Beauveria bassiana Growth, Development, and Virulence
by Qing Cai, Li Tian, Jia-Tao Xie, Dao-Hong Jiang and Nemat O. Keyhani
J. Fungi 2022, 8(3), 236; https://doi.org/10.3390/jof8030236 - 27 Feb 2022
Cited by 3 | Viewed by 2647
Abstract
Sirtuins are a class of histone deacetylases that promote heterochromatin formation to repress transcription. The entomopathogenic fungus Beauveria bassiana contains six sirtuin homologs. The class III histone deacetylase, BbSir2, has been previously shown to affect the regulation of carbon/nitrogen metabolism and asexual development, [...] Read more.
Sirtuins are a class of histone deacetylases that promote heterochromatin formation to repress transcription. The entomopathogenic fungus Beauveria bassiana contains six sirtuin homologs. The class III histone deacetylase, BbSir2, has been previously shown to affect the regulation of carbon/nitrogen metabolism and asexual development, with only moderate effects on virulence. Here, we examine another class III histone deacetylase (BbSirT2) and show that it contributes to deacetylation of lysine residues on histone H4-K16ac. Directed gene-knockout of BbSirT2 dramatically reduced conidiation, the ability of the fungus to metabolize a range of carbon and nitrogen sources, and tolerances to oxidative, heat, and UV stress and significantly attenuated virulence in both intrahemocoel injection and topical bioassays using the Greater wax moth (Galleria mellonella) as the insect host. ΔBbSirT2 cells showed alterations in cell cycle development and hyphal septation and produced morphologically aberrant conidia. Comparative transcriptomic analyses of wild type versus ΔBbSirT2 cells indicated differential expression of 1148 genes. Differentially expressed genes were enriched in pathways involved in cell cycle and rescue, carbon/nitrogen metabolism, and pathogenesis. These included changes in the expression of polyketide synthases (PKSs) and LysM effector proteins that contribute to degradation of host toxins and target host pathways, respectively. These data indicate contributions of BbSirT2 in helping to mediate fungal stress and development, with the identification of affected gene targets that can help account for the observed reduced virulence phenotype. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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12 pages, 2004 KiB  
Article
Screening and Identification of Indigenous Entomopathogenic Fungal Isolates from Agricultural Farmland Soils in Nile Delta, Egypt
by Alsayed Alfiky
J. Fungi 2022, 8(1), 54; https://doi.org/10.3390/jof8010054 - 05 Jan 2022
Cited by 10 | Viewed by 2730
Abstract
The compound negative impact of insect pests attacking agricultural ecosystems includes (i) direct yield losses from damaged crops, (ii) the economic cost of the attempt to prevent these losses and (iii) the negative short- and long-term hazard effects of chemical pesticides on human [...] Read more.
The compound negative impact of insect pests attacking agricultural ecosystems includes (i) direct yield losses from damaged crops, (ii) the economic cost of the attempt to prevent these losses and (iii) the negative short- and long-term hazard effects of chemical pesticides on human and environmental health. Entomopathogenic fungi (EMPF) are a group of microorganisms that represent the natural enemies of a number of crop pests, presenting an opportunity to harness their evolutionary fine-tuned relationship with their insect hosts as biocontrol agents in integrated pest management programs. The aim of this study was to establish an indigenous EMPF collection via the Galleria mellonella (greater wax moth) entrapment method from the soils of Nile Delta, Egypt. Obtained insect associated fungal isolates were bio-assayed for pathogenicity against the serious pest Spodoptera litura and Tenebrio molitor, and the seven outperforming isolates were selected for molecular identification and thermotolerance assay. Based on ITS sequence analysis and phylogeny, selected isolates were identified as Beauveria bassiana (four isolates), Metarhizium anisopliae (two isolates) and one isolate of Cordyceps javanica. The obtained results demonstrated (i) the efficacy of using insect baiting coupled with molecular identification and pathogenicity screening to isolate EMPF to control insect pests, and (ii) the availability of indigenous virulent EMPF in Nile Delta’s soil, which can be exploited for the development of sustainable crop protection strategies. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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11 pages, 595 KiB  
Article
Colonzation of Tobacco Plants by Fungal Entomopathogens and the Effect on Consumption over Diabrotica speciosa (Coleoptera: Chrysomelidae)
by Florencia Vianna, Sebastian Pelizza, Leticia Russo, Natalia Ferreri and Ana Clara Scorsetti
J. Fungi 2021, 7(12), 1017; https://doi.org/10.3390/jof7121017 - 27 Nov 2021
Cited by 1 | Viewed by 1735
Abstract
Entomopathogenic fungi are naturally occurring microorganisms that attack insect pests, making them exceptional allies when developing biocontrol strategies. A particular aspect of the ecology of these fungi is that they interact not only with insects but also with plants, being able to colonize [...] Read more.
Entomopathogenic fungi are naturally occurring microorganisms that attack insect pests, making them exceptional allies when developing biocontrol strategies. A particular aspect of the ecology of these fungi is that they interact not only with insects but also with plants, being able to colonize them endophytically without causing symptoms of disease. The objectives of this study were to determine the endophytic capacity of different species of entomopathogenic fungi in tobacco plants by means of foliar spraying, to evaluate the persistence in planta of the entomopathogens and the effect of endophytes on consumption by coleopteran pests. A total of 24 strains were analyzed to test endophytic capacity at 7, 14, 21 and 28 days post inoculation. A significant effect of the strains was found. On days 7, 14 and 21, the strain that showed the highest colonization percentages was B. bassiana LPSc 1215, and at day 28 B. bassiana strains LPSc 1215 and LPSc 1212 exhibited the best endophytic capacity, maintaining elevated colonization percentages. Choice test results indicated that D. speciosa fed indiscriminately on colonized and non-colonized leaves. The results indicate that B. bassiana LPSc 1215 constitutes a strain that would merit further investigation for the purpose of pest management in tobacco cultivation. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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10 pages, 1102 KiB  
Article
How Dopamine Influences Survival and Cellular Immune Response of Rhipicephalus microplus Inoculated with Metarhizium anisopliae
by Thaís Almeida Corrêa, Jéssica Fiorotti, Emily Mesquita, Laura Nóbrega Meirelles, Mariana Guedes Camargo, Caio Junior Balduino Coutinho-Rodrigues, Allan Felipe Marciano, Vânia Rita Elias Pinheiro Bittencourt and Patrícia Silva Golo
J. Fungi 2021, 7(11), 950; https://doi.org/10.3390/jof7110950 - 10 Nov 2021
Cited by 2 | Viewed by 1615
Abstract
Dopamine (DA) is a biogenic monoamine reported to modulate insect hemocytes. Although the immune functions of DA are known in insects, there is a lack of knowledge of DA’s role in the immune system of ticks. The use of Metarhizium anisopliae has been [...] Read more.
Dopamine (DA) is a biogenic monoamine reported to modulate insect hemocytes. Although the immune functions of DA are known in insects, there is a lack of knowledge of DA’s role in the immune system of ticks. The use of Metarhizium anisopliae has been considered for tick control, driving studies on the immune response of these arthropods challenged with fungi. The present study evaluated the effect of DA on the cellular immune response and survival of Rhipicephalus microplus inoculated with M. anisopliae blastospores. Exogenous DA increased both ticks’ survival 72 h after M. anisopliae inoculation and the number of circulating hemocytes compared to the control group, 24 h after the treatment. The phagocytic index of tick hemocytes challenged with M. anisopliae did not change upon injection of exogenous DA. Phenoloxidase activity in the hemolymph of ticks injected with DA and the fungus or exclusively with DA was higher than in untreated ticks or ticks inoculated with the fungus alone, 72 h after treatment. DA was detected in the hemocytes of fungus-treated and untreated ticks. Unveiling the cellular immune response in ticks challenged with entomopathogenic fungi is important to improve strategies for the biological control of these ectoparasites. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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15 pages, 885 KiB  
Article
Bioexploration and Phylogenetic Placement of Entomopathogenic Fungi of the Genus Beauveria in Soils of Lebanon Cedar Forests
by Charbel Al Khoury, Georges Nemer, Richard Humber, Nehme El-Hachem, Jacques Guillot, Racha Chehab, Elise Noujeim, Yara El Khoury, Wadih Skaff, Nathalie Estephan and Nabil Nemer
J. Fungi 2021, 7(11), 924; https://doi.org/10.3390/jof7110924 - 31 Oct 2021
Cited by 2 | Viewed by 2514
Abstract
The cedar forests of Lebanon have been threatened by the outbreak caused by climate change of a web-spinning sawfly, Cephalcia tannourinensis (Hymenoptera: Pamphiliidae), which negatively impacted the survival of one of the oldest tree species on earth. In this study, we investigated the [...] Read more.
The cedar forests of Lebanon have been threatened by the outbreak caused by climate change of a web-spinning sawfly, Cephalcia tannourinensis (Hymenoptera: Pamphiliidae), which negatively impacted the survival of one of the oldest tree species on earth. In this study, we investigated the occurrence of naturally soil-inhabiting entomopathogenic fungi for their role in containing the massive outbreak of this insect. We used a combination of fungal bioexploration methods, including insect bait and selective media. Morphological features and multilocus phylogeny—based on Sanger sequencing of the transcripts encoding the translation elongation factor 1-alpha (TEF-α), RNA polymerase II second largest subunit (RBP2), and the nuclear intergenic region (Bloc) were used for species identification. The occurrence rate of entomopathogenic fungi (EPF) varied with location, soil structure, forest structure, and isolation method. From 15 soil samples positive for fungal occurrence, a total of 249 isolates was obtained from all locations using different isolation methods. The phylogenetic analysis confirmed the existence of two novel indigenous species: Beauveria tannourinensis sp. nov. and Beauveria ehdenensis sp. nov. In conclusion, the present survey was successful (1) in optimizing the isolation methods for EPF, (2) investigating the natural occurrence of Beauveria spp. in outbreak areas of C. tannourinensis, and (3) in characterizing the presence of new Beauveria species in Lebanese cedar forest soil. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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20 pages, 3308 KiB  
Article
The Spt10 GNAT Superfamily Protein Modulates Development, Cell Cycle Progression and Virulence in the Fungal Insect Pathogen, Beauveria bassiana
by Qing Cai, Juan-Juan Wang, Jia-Tao Xie, Dao-Hong Jiang and Nemat O. Keyhani
J. Fungi 2021, 7(11), 905; https://doi.org/10.3390/jof7110905 - 26 Oct 2021
Cited by 6 | Viewed by 2079
Abstract
Chromatin remodeling is mediated in part by post-translational acetylation/deacetylation modifications of histones. Histone acetyltransferases (HATs), e.g., members of the GNAT/MYST superfamily, activate gene transcription via promotion of euchromatin formation. Here, we characterized a GNAT family HAT, Spt10 (BbSpt10), in the environmentally and economically [...] Read more.
Chromatin remodeling is mediated in part by post-translational acetylation/deacetylation modifications of histones. Histone acetyltransferases (HATs), e.g., members of the GNAT/MYST superfamily, activate gene transcription via promotion of euchromatin formation. Here, we characterized a GNAT family HAT, Spt10 (BbSpt10), in the environmentally and economically important fungal insect pathogen, Beauveria bassiana. Targeted gene knockout of BbSpt10 resulted in impaired asexual development and morphogenesis; reduced abilities to utilize various carbon/nitrogen sources; reduced tolerance to heat, fungicides, and DNA damage stress; and attenuated virulence. The ΔBbSpt10 mutant showed disrupted cell cycle development and abnormal hyphal septation patterns. Transcriptome analyses of wild type and ΔBbSpt10 cells revealed the differential expression of 373 genes, including 153 downregulated and 220 upregulated genes. Bioinformatic analyses revealed downregulated genes to be enriched in pathways involved in amino acid metabolism, cellular transportation, cell type differentiation, and virulence, while upregulated genes were enriched in carbon/nitrogen metabolism, lipid metabolism, DNA process, and cell rescue, defense, and virulence. Downregulated virulence genes included hydrophobins, cellular transporters (ABC and MFS multidrug transporters) and cytochrome P450 detoxification genes. These data indicated broad effects of BbSpt10 on fungal development, multi-stress response, and virulence. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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20 pages, 2774 KiB  
Article
Genome-Wide Insight into Profound Effect of Carbon Catabolite Repressor (Cre1) on the Insect-Pathogenic Lifecycle of Beauveriabassiana
by Rehab Abdelmonem Mohamed, Kang Ren, Ya-Ni Mou, Sheng-Hua Ying and Ming-Guang Feng
J. Fungi 2021, 7(11), 895; https://doi.org/10.3390/jof7110895 - 23 Oct 2021
Cited by 7 | Viewed by 1631
Abstract
Carbon catabolite repression (CCR) is critical for the preferential utilization of glucose derived from environmental carbon sources and regulated by carbon catabolite repressor A (Cre1/CreA) in filamentous fungi. However, a role of Cre1-mediated CCR in insect-pathogenic fungal utilization of host nutrients during normal [...] Read more.
Carbon catabolite repression (CCR) is critical for the preferential utilization of glucose derived from environmental carbon sources and regulated by carbon catabolite repressor A (Cre1/CreA) in filamentous fungi. However, a role of Cre1-mediated CCR in insect-pathogenic fungal utilization of host nutrients during normal cuticle infection (NCI) and hemocoel colonization remains explored insufficiently. Here, we report an indispensability of Cre1 for Beauveriabassiana’s utilization of nutrients in insect integument and hemocoel. Deletion of cre1 resulted in severe defects in radial growth on various media, hypersensitivity to oxidative stress, abolished pathogenicity via NCI or intrahemocoel injection (cuticle-bypassing infection) but no change in conidial hydrophobicity and adherence to insect cuticle. Markedly reduced biomass accumulation in the Δcre1 cultures was directly causative of severe defect in aerial conidiation and reduced secretion of various cuticle-degrading enzymes. The majority (1117) of 1881 dysregulated genes identified from the Δcre1 versus wild-type cultures were significantly downregulated, leading to substantial repression of many enriched function terms and pathways, particularly those involved in carbon and nitrogen metabolisms, cuticle degradation, antioxidant response, cellular transport and homeostasis, and direct/indirect gene mediation. These findings offer a novel insight into profound effect of Cre1 on the insect-pathogenic lifestyle of B. bassiana. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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18 pages, 2270 KiB  
Article
Beauveria bassiana Xylanase: Characterization and Wastepaper Deinking Potential of a Novel Glycosyl Hydrolase from an Endophytic Fungal Entomopathogen
by Ayodeji Amobonye, Prashant Bhagwat, Suren Singh and Santhosh Pillai
J. Fungi 2021, 7(8), 668; https://doi.org/10.3390/jof7080668 - 18 Aug 2021
Cited by 10 | Viewed by 2650
Abstract
Beauveria bassiana is an entomopathogenic fungus widely used as a biopesticide for insect control; it has also been shown to exist as an endophyte, promoting plant growth in many instances. This study highlights an alternative potential of the fungus; in the production of [...] Read more.
Beauveria bassiana is an entomopathogenic fungus widely used as a biopesticide for insect control; it has also been shown to exist as an endophyte, promoting plant growth in many instances. This study highlights an alternative potential of the fungus; in the production of an industrially important biocatalyst, xylanase. In this regard, Beauveria bassiana SAN01 xylanase was purified to homogeneity and subsequently characterized. The purified xylanase was found to have a specific activity of 324.2 U·mg−1 and an estimated molecular mass of ~37 kDa. In addition, it demonstrated optimal activity at pH 6.0 and 45 °C while obeying Michaelis–Menton kinetics towards beechwood xylan with apparent Km, Vmax and kcat of 1.98 mg·mL−1, 6.65 μM·min−1 and 0.62 s−1 respectively. The enzyme activity was strongly inhibited by Ag2+ and Fe3+ while it was significantly enhanced by Co2+ and Mg2+. Furthermore, the xylanase was shown to effectively deink wastepaper at an optimal rate of 106.72% through its enzymatic disassociation of the fiber-ink bonds as demonstrated by scanning electron microscopy and infrared spectroscopy. This is the first study to demonstrate the biotechnological application of a homogeneously purified glycosyl hydrolase from B. bassiana. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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Review

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9 pages, 587 KiB  
Review
The Entomopathogenic Fungus Beauveria bassiana Shows Its Toxic Side within Insects: Expression of Genes Encoding Secondary Metabolites during Pathogenesis
by Nicolás Pedrini
J. Fungi 2022, 8(5), 488; https://doi.org/10.3390/jof8050488 - 07 May 2022
Cited by 21 | Viewed by 4619
Abstract
Entomopathogenic fungi are extensively used for the control of insect pests worldwide. Among them, Beauveria bassiana (Ascomycota: Hypocreales) produce a plethora of toxic secondary metabolites that either facilitate fungal invasion or act as immunosuppressive compounds. These toxins have different chemical natures, such as [...] Read more.
Entomopathogenic fungi are extensively used for the control of insect pests worldwide. Among them, Beauveria bassiana (Ascomycota: Hypocreales) produce a plethora of toxic secondary metabolites that either facilitate fungal invasion or act as immunosuppressive compounds. These toxins have different chemical natures, such as nonribosomal peptides and polyketides. Even though their precise role is poorly understood, they are usually linked to virulence. These fungal secondary metabolites are produced by the expression of gene clusters encoding the various proteins needed for their biosynthesis. Each cluster includes synthetases for nonribosomal peptides (NRPS), polyketides (PKS), or hybrid NRPS–PKS genes. The aim of this review is to summarize the information available from transcriptomics and quantitative PCR studies related to the expression of B. bassiana NRPS and PKS genes inside different insects as the infection progresses; as for the host immune response, to help understand the mechanisms that these toxins trigger as virulence factors, antimicrobials, or immunosuppressives within the context of a fungus–insect interaction. Full article
(This article belongs to the Special Issue The Multifaceted Beauveria bassiana and Other Insect-Related Fungi)
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