Population genomics and evolution of a fungal pathogen after releasing exotic strains to control insect pests for 20 years

Mei, Lijuan; Chen, Mingjun; Shang, Yanfang; Tang, Gong‐Jian; Tao, Ye; Zeng, Liang; Huang, Bo; Li, Zengzhi; Zhan, Shuai; Wang, Chengshu

doi:10.1038/s41396-020-0620-8

Cited by 31 publications

(24 citation statements)

References 57 publications

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“…Mei at el. [ 154 ] reported on the ecological and evolutionary scenario of the Beauveria population genomics over 20 years after releasing exotic strains to control pine caterpillar pests. They found that the population was largely clonal in nature and the released strains could persist in the field for a long time (20 years) but with low recovery rates.…”

Section: Genomic Advances In Ascomycotamentioning

confidence: 99%

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An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota

Muggia

Ametrano

Sterflinger

et al. 2020

Life

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Fungi are among the most successful eukaryotes on Earth: they have evolved strategies to survive in the most diverse environments and stressful conditions and have been selected and exploited for multiple aims by humans. The characteristic features intrinsic of Fungi have required evolutionary changes and adaptations at deep molecular levels. Omics approaches, nowadays including genomics, metagenomics, phylogenomics, transcriptomics, metabolomics, and proteomics have enormously advanced the way to understand fungal diversity at diverse taxonomic levels, under changeable conditions and in still under-investigated environments. These approaches can be applied both on environmental communities and on individual organisms, either in nature or in axenic culture and have led the traditional morphology-based fungal systematic to increasingly implement molecular-based approaches. The advent of next-generation sequencing technologies was key to boost advances in fungal genomics and proteomics research. Much effort has also been directed towards the development of methodologies for optimal genomic DNA and protein extraction and separation. To date, the amount of proteomics investigations in Ascomycetes exceeds those carried out in any other fungal group. This is primarily due to the preponderance of their involvement in plant and animal diseases and multiple industrial applications, and therefore the need to understand the biological basis of the infectious process to develop mechanisms for biologic control, as well as to detect key proteins with roles in stress survival. Here we chose to present an overview as much comprehensive as possible of the major advances, mainly of the past decade, in the fields of genomics (including phylogenomics) and proteomics of Ascomycota, focusing particularly on those reporting on opportunistic pathogenic, extremophilic, polyextremotolerant and lichenized fungi. We also present a review of the mostly used genome sequencing technologies and methods for DNA sequence and protein analyses applied so far for fungi.

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Section: Genomic Advances In Ascomycotamentioning

confidence: 99%

“…With this study Mei at el. [ 154 ] paved the way for researches on population evolution of other species of entomopathogens, especially for biocontrol species with narrow host ranges.…”

Section: Genomic Advances In Ascomycotamentioning

confidence: 99%

An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota

Muggia

Ametrano

Sterflinger

et al. 2020

Life

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“…It is therefore conceivable that the multiple species or strain spores of fungal parasites can land on individual insect hosts to theoretically trigger co-infections. In reality, however, the insect cadavers collected from the fields are always mycosed by a single species/strain of fungal parasites [ 7 , 8 ]. On the other hand, coenzootic or coepizootic fungal insect diseases have been frequently observed in the field, where the same or different species of insects were killed and mycosed by different strains or species of fungal parasites [ 8 , 9 , 10 ].…”

Section: Introductionmentioning

confidence: 99%

“…Field application and recovery studies revealed that the inundative application of mycoinsecticide agents such as B. bassiana did not displace local population. Instead, different genotypic strains coexist in the field by infection of different insects, and less than 3% of the insect cadavers were mycosed by the released strains [ 7 , 21 ]. These kinds of studies have not investigated the effect of biocontrol releases on other species of fungal parasites.…”

Section: Introductionmentioning

confidence: 99%

Empirical Support for the Pattern of Competitive Exclusion between Insect Parasitic Fungi

Chen

et al. 2021

JoF

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Fungal entomopathogens are largely facultative parasites and play an important role in controlling the density of insect populations in nature. A few species of these fungi have been used for biocontrol of insect pests. The pattern of the entomopathogen competition for insect individuals is still elusive. Here, we report the empirical competition for hosts or niches between the inter- and intra-species of the entomopathogens Metarhizium robertsii and Beauveria bassiana. It was found that the synergistic effect of coinfection on virulence increase was not evident, and the insects were largely killed and mycosed by M. robertsii independent of its initial co-inoculation dosage and infection order. For example, >90% dead insects were mycosed by M. robertsii even after immersion in a spore suspension with a mixture ratio of 9:1 for B. bassiana versus M. robertsii. The results thus support the pattern of competitive exclusion between insect pathogenic fungi that occurred from outside to inside the insect hosts. Even being inferior to compete for insects, B. bassiana could outcompete M. robertsii during co-culturing in liquid medium. It was also found that the one-sided mycosis of insects occurred during coinfection with different genotypic strains of either fungi. However, parasexual recombination was evident to take place between the compatible strains after coinfection. The data of this study can help explain the phenomena of the exclusive mycosis of insect individuals, but co-occurrence of entomopathogens in the fields, and suggest that the synergistic effect is questionable regarding the mixed use of fungal parasites for insect pest control.

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“…Contrary to that in Beauveria species (25), it is easy to induce sexual fruiting bodies for C. militaris (20). Thus, the fruiting bodies of C. militaris were induced both on silk moth pupae and rice medium (see Fig.…”

Section: Resultsmentioning

confidence: 87%

Production of Diverse Beauveriolide Analogs in Closely Related Fungi: a Rare Case of Fungal Chemodiversity

Yin

Chen

Song

et al. 2020

mSphere

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Fungal chemodiversity is well known in part due to the production of diverse analogous compounds by a single biosynthetic gene cluster (BGC). Usually, similar or the same metabolites are produced by closely related fungal species under a given condition, the foundation of fungal chemotaxonomy. Here, we report a rare case of the production of the cyclodepsipeptide beauveriolides (BVDs) in three insect-pathogenic fungi. We found that the more closely related fungi Beauveria bassiana and Beauveria brongniartii produced structurally distinct analogs of BVDs, whereas the less-close relatives B. brongniartii and Cordyceps militaris biosynthesized structurally similar congeners under the same growth condition. It was verified that a conserved BGC containing four genes is responsible for BVD biosynthesis in three fungi, including a polyketide synthase (PKS) for the production of 3-hydroxy fatty acids (FAs) with chain length variations. In contrast to BVD production patterns, phylogenetic analysis of the BGC enzymes or enzyme domains largely resulted in the congruence relationship with fungal speciation. Feeding assays demonstrated that an FA with a chain length of eight carbon atoms was preferentially utilized, whereas an FA with a chain longer than 10 carbon atoms could not be used as a substrate for BVD biosynthesis. Insect survival assays suggested that the contribution of BVDs to fungal virulence might be associated with the susceptibility of insect species. The results of this study enrich the knowledge of fungal secondary metabolic diversity that can question the reliability of fungal chemotaxonomy. IMPORTANCE Fungal chemotaxonomy is an approach to classify fungi based on the fungal production profile of metabolites, especially the secondary metabolites. We found an atypical example that could question the reliability of fungal chemical classifications in this study, i.e., the more closely related entomopathogenic species Beauveria bassiana and Beauveria brongniartii produced structurally different congeners of the cyclodepsipeptide beauveriolides, whereas the rather divergent species B. brongniartii and Cordyceps militaris biosynthesized similar analogs under the same growth condition. The conserved biosynthetic gene cluster (BGC) containing four genes present in each species is responsible for beauveriolide production. In contrast to the compound formation profiles, the phylogenies of biosynthetic enzymes or enzymatic domains show associations with fungal speciation. Dependent on the insect species, production of beauveriolides may contribute to fungal virulence against the susceptible insect hosts. The findings in this study augment the diversity of fungal secondary metabolisms.

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Population genomics and evolution of a fungal pathogen after releasing exotic strains to control insect pests for 20 years

Cited by 31 publications

References 57 publications

An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota

An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota

Empirical Support for the Pattern of Competitive Exclusion between Insect Parasitic Fungi

Production of Diverse Beauveriolide Analogs in Closely Related Fungi: a Rare Case of Fungal Chemodiversity

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