Production of Helvolic Acid in Metarhizium Contributes to Fungal Infection of Insects by Bacteriostatic Inhibition of the Host Cuticular Microbiomes

Sun, Yanlei; Chen, Haimin; Yin, Ying; Wang, Chengshu

doi:10.1128/spectrum.02620-22

Cited by 17 publications

(8 citation statements)

References 54 publications

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“…Multiple mechanisms may be involved in this phenomenon. In particular, M. robertsii is known to produce diverse antimicrobial metabolites (helvolic acid, ustilaginoidin, pseurotin, indigotide, and hydroxy-ovalicin) to suppress bacteria ( Sun et al, 2022a , 2022b ). Moreover, the spectrum of volatile organic compounds emitted by Metarhizium fungi inhibits the development of competing bacteria and fungi, including phytopathogenic ones ( Hummadi et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Effects of passages through an insect or a plant on virulence and physiological properties of the fungus Metarhizium robertsii

Tomilova,

Kryukov,

Kryukova

et al. 2023

PeerJ

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Species of the genus Metarhizium are characterized by a multitrophic lifestyle of being arthropod parasites, rhizosphere colonizers, endophytes, and saprophytes. The process of adaptation to various organisms and substrates may lead to specific physiological alterations that can be elucidated by passaging through different hosts. Changes in virulence and cultivation properties of entomopathogenic fungi subcultured on different media or passaged through a live insect host are well known. Nevertheless, comparative in-depth physiological studies on fungi after passaging through insect or plant organisms are scarce. Here, virulence, plant colonization, hydrolytic enzymatic activities, toxin production, and antimicrobial action were compared between stable (nondegenerative) parent strain Metarhizium robertsii MB-1 and its reisolates obtained after eight passages through Galleria mellonella larvae or Solanum lycopersicum or after subculturing on the Sabouraud medium. The passaging through the insect caused similar physiological alterations relative to the plant-based passaging: elevation of destruxin A, B, and E production, a decrease in protease and lipase activities, and lowering of virulence toward G. mellonella and Leptinotarsa decemlineata as compared to the parent strain. The reisolates passaged through the insect or plant showed a slight trend toward increased tomato colonization and enhanced antagonistic action on tomato-associated bacterium Bacillus pumilus as compared to the parental strain. Meanwhile, the subculturing of MB-1 on the Sabouraud medium showed stability of the studied parameters, with minimal alterations relative to the parental strain. We propose that the fungal virulence factors are reprioritized during adaptation of M. robertsii to insects, plants, and media.

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Section: Discussionmentioning

confidence: 99%

Effects of passages through an insect or a plant on virulence and physiological properties of the fungus Metarhizium robertsii

Tomilova,

Kryukov,

Kryukova

et al. 2023

PeerJ

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“…The collected insects were anesthetized on ice for 1 h, and three insects were used as a replicate by washing and vortexing in 50 ml phosphate buffer solution (PBS; pH, 7.0) for 30 s. The washing buffers were diluted properly (500 × for L4E and L5D6 samples; 100 × for L5D3 sample; no dilution for L5D0 sample) for inoculation of LB plates, Marine agar (Biofeng), and GYC plates (glucose, 50 g/l; yeast extract, 10 g/l; 0.5% CaCO 3 , 5 g/l; agar, 15 g/l) for 2 days at 30 ℃ to count bacterial colony forming units (CFUs), which were converted to the unit of CFUs per insect [ 31 ]. The antibiotic specifically inhibiting the Gram-positive (G + ; Nafcillin, Topscience, Shanghai) and Gram-negarive (G − ; Aztreonam, Qisong Biotech, Beijing) bacteria were added to LB medium at a final concentration of 50 μg/ml to determine the numbers of the G + /G − bacterial CFUs [ 30 ], respectively. There were 10 replicates for each age of insects, and a two-tailed Student’s t- test was conducted to compare the difference in CFU numbers between different ages of insects using the program GraphPad (ver.…”

Section: Methodsmentioning

confidence: 99%

“…In contrast to the per os infection by pathogenic bacteria and viruses, fungal parasites infect insects via penetration of cuticles [ 28 , 29 ]. Insect cuticular bacteria can thus mediate colonization resistance against EPF such as M. robertsii and B. bassiana by inhibiting fungal spore germination and or infection structure differentiation [ 6 , 30 ]. The ectomicrobiotas of silkworm larvae are unclear and it is also unknown whether its cuticle bacteria could help improve insect survival against fungal parasite infections.…”

Section: Introductionmentioning

confidence: 99%

“…For example, to counteract the resistance of insect cuticular bacteria, B. bassiana secrets a defensin-like antibacterial peptide that can kill diverse bacteria, especially Gram-positive bacteria [ 31 ]. M. robertsii , however, produces different potent antibiotic compounds to combat different bacteria to facilitate fungal infection of insects or growth in diverse environments [ 30 , 32 ]. Likewise, different bacteria can produce diverse antifungal metabolites or enzymes (e.g., lysozymes) [ 33 ].…”

Section: Introductionmentioning

confidence: 99%

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From phyllosphere to insect cuticles: silkworms gather antifungal bacteria from mulberry leaves to battle fungal parasite attacks

Zhao,

Hong,

et al. 2024

Microbiome

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Background Bacterial transfers from plants to insect herbivore guts have been well investigated. However, bacterial exchanges between plant phyllospheres and insect cuticles remain unclear, as does their related biological function. Results Here, we report that the cuticular bacterial loads of silkworm larvae quickly increased after molting and feeding on the white mulberry (Morus alba) leaves. The isolation and examination of silkworm cuticular bacteria identified one bacterium Mammaliicoccus sciuri that could completely inhibit the spore germination of fungal entomopathogens Metarhizium robertsii and Beauveria bassiana. Interestingly, Ma. sciuri was evident originally from mulberry leaves, which could produce a secreted chitinolytic lysozyme (termed Msp1) to damage fungal cell walls. In consistency, the deletion of Msp1 substantially impaired bacterial antifungal activity. Pretreating silkworm larvae with Ma. sciuri cells followed by fungal topical infections revealed that this bacterium could help defend silkworms against fungal infections. Unsurprisingly, the protective efficacy of ΔMsp1 was considerably reduced when compared with that of wild-type bacterium. Administration of bacterium-treated diets had no negative effect on silkworm development; instead, bacterial supplementation could protect the artificial diet from Aspergillus contamination. Conclusions The results of this study evidence that the cross-kingdom transfer of bacteria from plant phyllospheres to insect herbivore cuticles can help protect insects against fungal parasite attacks.

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“…The treatments with 0.05% Tween was included as mock controls. The survival-curve difference of insects after treated with different strains were compared by Kaplan–Meier analysis ( 56 ).…”

Section: Methodsmentioning

confidence: 99%

A bacterial-like Pictet–Spenglerase drives the evolution of fungi to produce β-carboline glycosides together with separate genes

Sun

Yin

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Diverse β-carboline (βC) alkaloids are produced by microbes, plants, and animals with myriad bioactivities and drug potentials. However, the biosynthetic mechanism of βCs remains largely elusive, especially regarding the hydroxyl and glucosyl modifications of βCs. Here, we report the presence of the bacterial-like Pictet–Spenglerase gene Fcs1 in the entomopathogenic Beauveria fungi that can catalyze the biosynthesis of the βC skeleton. The overexpression of Fcs1 in Beauveria bassiana led to the identification of six βC methyl glycosides, termed bassicarbosides (BCSs) A–F. We verified that the cytochrome P450 (CYP) genes adjacent to Fcs1 cannot oxidize βCs. Alternatively, the separated CYP684B2 family gene Fcs2 was identified to catalyze βC hydroxylation together with its cofactor gene Fcs3 . The functional homologue of Fcs2 is only present in the Fcs1- containing fungi and highly similar to the Fcs1- connected yet nonfunctional CYP. Both evolved quicker than those from fungi without Fcs1 homologues. Finally, the paired methyl/glucosyl transferase genes were verified to mediate the production of BCSs from hydroxy-βCs. All these functionally verified genes are located on different chromosomes of Beauveria , which is in contrast to the typical content-clustered feature of fungal biosynthetic gene clusters (BGCs). We also found that the production of BCSs selectively contributed to fungal infection of different insect species. Our findings shed light on the biosynthetic mechanism of βC glycosides, including the identification of a βC hydroxylase. The results of this study also propose an evolving process of fungal BGC formation following the horizontal transfer of a bacterial gene to fungi.

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Production of Helvolic Acid in Metarhizium Contributes to Fungal Infection of Insects by Bacteriostatic Inhibition of the Host Cuticular Microbiomes

Cited by 17 publications

References 54 publications

Effects of passages through an insect or a plant on virulence and physiological properties of the fungus Metarhizium robertsii

Effects of passages through an insect or a plant on virulence and physiological properties of the fungus Metarhizium robertsii

From phyllosphere to insect cuticles: silkworms gather antifungal bacteria from mulberry leaves to battle fungal parasite attacks

A bacterial-like Pictet–Spenglerase drives the evolution of fungi to produce β-carboline glycosides together with separate genes

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