Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana - PubMed (original) (raw)

Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana

Guohua Xiao et al. Sci Rep. 2012.

Abstract

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 pathogenicity. We also found many species-specific virulence genes and gene family expansions and contractions that correlate with host ranges and pathogenic strategies. These include B. bassiana having many more bacterial-like toxins (suggesting an unsuspected potential for oral toxicity) and effector-type proteins. The genome also revealed that B. bassiana resembles the closely related Cordyceps militaris in being heterothallic, although its sexual stage is rarely observed. A high throughput RNA-seq transcriptomic analysis revealed that B. bassiana could sense and adapt to different environmental niches by activating well-defined gene sets. The information from this study will facilitate further development of B. bassiana as a cost-effective mycoinsecticide.

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Figures

Figure 1

Figure 1. Comparative genomics analysis of three insect pathogens.

(A) Functional classification and comparison of B. bassiana (Bb), C. militaris (Cm) and M. robertsii (Mr) proteins. Each circle represents the relative fraction of genes represented in each of the categories for each genome. (B) Reciprocal blast analysis of the predicted proteins among the three insect pathogens. The cut-off E value is at ≤ 1e-5.

Figure 2

Figure 2. Comparative genomics and phylogenomic analyses of B. bassiana with other fungi.

(A) Scatter plots of Blast score ratio analysis of B. bassiana (Bb), C. militaris (Cm) and M. robertsii (Mr) showing that Bb is more closely related to Cm. The numbers in red in the lower left corners indicate the percentages of Bb species-specific sequences and the numbers in the upper left or lower right show the percentages of lineage-specific genes between pairs of genomes as indicated. (B) A maximum likelihood phylogenomic tree constructed using the Dayhoff amino acid substitution model showing the evolutionary relationship of Bb with other fungal species. (C) Phenotypic and morphological comparison of Bb and Cm. Panel 1, a wax moth (Galleria mellonella) larva killed and mycosed by Bb; Panel 2, Cm fruits on a silkworm (Bombyx mori) pupa; Panel 3, Bb conidial formation on a zig-zag shared conidiophore; Panel 4, Cm conidial formation on a phialide-type conidiophore; Panel 5, a Bb germ tube on a locust hind wing showing tip swelling; Panel 6, a Cm germ tube on a locust hind wing without tip swelling; Panel 7, Bb hyphal bodies harvested from cotton bollworm 48 hrs post infection; Panel 8, a perithecium produced on the Cm fruiting body_._

Figure 3

Figure 3. Comparative genomic analysis.

(A) Dot blot analysis of B. bassiana and C. militaris genome structures using ordered scaffold data. (B) Distribution of paralogous genes with different levels of nucleotide similarity in B. bassiana (highlighted in red) and other fungi. (C) Syntenic relationships of the MAT loci and their flanking regions between B. bassiana (Bb), C. militaris (Cm), M. robertsii (Mr) and M. acridum (Ma). Loci in the same color show orthologous relationships.

Figure 4

Figure 4. Growth tests.

Conidial suspensions (2.5 μl) of B. bassiana (Bb), C. militaris (Cm) and M. robertsii (Mr) were inoculated onto minimal medium supplemented with 1% xylose (A) or 1% glucose (B) and incubated for 10 days at 25°C. In contrast to Mr, Cm failed to grow on xylose medium while Bb germinated and grew poorly.

Figure 5

Figure 5. RNA-seq analysis of differentially expressed genes by B. bassiana adapting to different environmental niches.

(A) Summary of significantly up- and down-regulated genes between different libraries. (B) Venn diagram analysis of co-expressed genes in different libraries. The numbers in parenthesis show total expressed genes with more than two transcripts. The numbers in square brackets show those of the 100 most highly expressed genes. (C) Heat map of the transcription factors differentially expressed by Bb in different conditions. The fungus was harvested from cotton bollworm hemocoel (CB), locust hind wings (LW) and corn root exudates (RE) for RNA extraction and RNA-seq analysis (TPM, transcripts per million tags).

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