Comparative genome and transcriptome analysis of the nematode-trapping fungus Duddingtonia flagrans reveals high pathogenicity during nematode infection

Zhang, Wei; Liu, Dandan; Yu, Zhichao; Hou, Bin; Fan, Yixing; Li, Zehao; Shang, Shijie; Qiao, Yidan; Fu, Jiang‐Tao; Niu, Jiekang; Li, Bin; Duan, Kexin; XiaoYe, Yang; Wang, Rui

doi:10.1016/j.biocontrol.2019.104159

Cited by 8 publications

(6 citation statements)

References 68 publications

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“…The extracellular adhesive layer of traps is essential for nematode capture. Three types of adhesive proteins, including those containing GLEYA (PF10528), Egh16-like (PF11327), and CFEM (PF05730), were predicted to be involved in capturing nematodes (Liang et al 2015; Ji et al 2020; Zhang et al 2020). These adhesive proteins accounted for more than 2% of the secreted proteins in all NTF, which is higher than that in non-NTF (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Similarly, the genes of cell-surface proteins containing the carbohydrate-binding WSC domain were up-regulated during nematode infection (Andersson et al 2013; 2014) and were found to be significantly expanded in NTF (Supplementary Table 9). Other expanded gene families that may be linked to fungal carnivorism are those encoding adhesive proteins and proteases such as subtilase (Liang et al 2015; Wang et al 2015; Ji et al 2020; Zhang et al 2020). Overall, the patterns of gene family expansion in NTF resemble those observed in plant pathogens rather than patterns found in insect and animal pathogens (Meerupati et al 2013).…”

Section: Discussionmentioning

confidence: 99%

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The Genomes of Nematode-Trapping Fungi Provide Insights into the Origin and Diversification of Fungal Carnivorism

Fan,

Du,

Zhang

et al. 2024

Preprint

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Nematode-trapping fungi (NTF), most of which belong to a monophyletic lineage in Ascomycota, cannibalize nematodes and other microscopic animals, raising questions regarding the types and mechanisms of genomic changes that enabled carnivorism and adaptation to the carbon-rich and nitrogen-poor environment created by the Permian-Triassic extinction event. Here, we conducted comparative genomic analyses of 21 NTF and 21 non-NTF to address these questions. Carnivorism-associated changes include expanded genes for nematode capture, infection, and consumption (e.g., adhesive proteins, CAP superfamily, eukaryotic aspartyl proteases, and serine-type peptidases). Although the link between secondary metabolite (SM) production and carnivorism remains unclear, we found that the numbers of SM gene clusters among NTF are significantly lower than those among non-NTF. Significantly expanded cellulose degradation gene families (GH5, GH7, AA9, and CBM1) and contracted genes for carbon-nitrogen hydrolases (enzymes that degrade organic nitrogen to ammonia) are likely associated with adaptation to the carbon-rich and nitrogen-poor environment. Through horizontal gene transfer events from bacteria, NTF acquired the Mur gene cluster (participating in synthesizing peptidoglycan of the bacterial cell wall) and Hyl (a virulence factor in animals). Disruption of MurE reduced NTF's ability to attract nematodes, supporting its role in carnivorism. This study provides new insights into how NTF evolved and diversified after the Permian-Triassic mass extinction event.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The Genomes of Nematode-Trapping Fungi Provide Insights into the Origin and Diversification of Fungal Carnivorism

Fan,

Du,

Zhang

et al. 2024

Preprint

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“…Experimental studies in vitro have shown that D. flagrans could reduce up to 96.4% of GINs, better than Monacrosporium thaumasium and Arthrobotrys robusta [41,42], and in in vivo tests a reduction of 55.15%-98.82% has been reported [43]. With the development of next-generation sequencing, genomic analysis of D. flagrans has shown that the species contains more abundant genes relating to the pathogenicity of nematodes than other fungi, such as cytochrome P450 genes and proteasecoding genes, which provide D. flagrans with stronger nematicidal activity and keep other enemies (such as fungal-feeding nematodes) from feeding [44,45]. Moreover, D. flagrans has fewer carbohydrate-degradation-related genes and a weaker saprophytic capability than other fungi, which makes D. flagrans rely on nematodes as its sole nutrition source, which is associated with its excellent ability to form traps [44,46].…”

Section: Duddingtoniamentioning

confidence: 99%

“…With the development of next-generation sequencing, genomic analysis of D. flagrans has shown that the species contains more abundant genes relating to the pathogenicity of nematodes than other fungi, such as cytochrome P450 genes and proteasecoding genes, which provide D. flagrans with stronger nematicidal activity and keep other enemies (such as fungal-feeding nematodes) from feeding [44,45]. Moreover, D. flagrans has fewer carbohydrate-degradation-related genes and a weaker saprophytic capability than other fungi, which makes D. flagrans rely on nematodes as its sole nutrition source, which is associated with its excellent ability to form traps [44,46]. To date, D. flagrans has been viewed as a good controller of trichostrongylides and cyathostome (the most prevalent GINs in livestock) in various domestic animals (Table 1).…”

Section: Duddingtoniamentioning

confidence: 99%

Individual and Combined Application of Nematophagous Fungi as Biological Control Agents against Gastrointestinal Nematodes in Domestic Animals

Gong

et al. 2022

Pathogens

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Gastrointestinal nematodes (GINs) are a group of parasites that threaten livestock yields, and the consequent economic losses have led to major concern in the agricultural industry worldwide. The high frequency of anthelmintic resistance amongst GINs has prompted the search for sustainable alternatives. Recently, a substantial number of both in vitro and in vivo experiments have shown that biological controls based on predatory fungi and ovicidal fungi are the most promising alternatives to chemical controls. In this respect, the morphological characteristics of the most representative species of these two large groups of fungi, their nematicidal activity and mechanisms of action against GINs, have been increasingly studied. Given the limitation of the independent use of a single nematophagous fungus (NF), combined applications which combine multiple fungi, or fungi and chemical controls, have become increasingly popular, although these new strategies still have antagonistic effects on the candidates. In this review, we summarize both the advantages and disadvantages of the individual fungi and the combined applications identified to date to minimize recurring infections or to disrupt the life cycle of GINs. The need to discover novel and high-efficiency nematicidal isolates and the application of our understanding to the appropriate selection of associated applications are discussed.

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“…The biocontrol ability of B. bassiana’s infection of Tenebrio molitor larvae and adults and G. mellonella larvae was influenced after the PacC TF gene pacC was disrupted [ 112 ]. The Zn(2)-C6-type transcription factor-encoding gene was upregulated in Duddingtonia flagrans, infecting nematodes at different trapping stages [ 113 ]. In C. minitans , deletion of the PacC TF gene CmpacC reduced the mycoparasitic activity of C. minitans against S. sclerotiorum and the activities of the cell-wall-degrading enzymes chitinase and β-1,3-glucanase [ 114 ].…”

Section: Transcription Factorsmentioning

confidence: 99%

cAMP Signalling Pathway in Biocontrol Fungi

Sun

Wang

2022

CIMB

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Biocontrol is a complex process, in which a variety of physiological and biochemical characteristics are altered. The cAMP signalling pathway is an important signal transduction pathway in biocontrol fungi and consists of several key components. The G-protein system contains G-protein coupled receptors (GPCRs), heterotrimeric G-proteins, adenylate cyclase (AC), cAMP-dependent protein kinase (PKA), and downstream transcription factors (TFs). The cAMP signalling pathway can regulate fungal growth, development, differentiation, sporulation, morphology, secondary metabolite production, environmental stress tolerance, and the biocontrol of pathogens. However, few reviews of the cAMP signalling pathway in comprehensive biocontrol processes have been reported. This work reviews and discusses the functions and applications of genes encoding each component in the cAMP signalling pathway from biocontrol fungi, including the G-protein system components, AC, PKA, and TFs, in biocontrol behaviour. Finally, future suggestions are provided for constructing a complete cAMP signalling pathway in biocontrol fungi containing all the components and downstream effectors involved in biocontrol behavior. This review provides useful information for the understanding the biocontrol mechanism of biocontrol fungi by utilising the cAMP signalling pathway.

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Comparative genome and transcriptome analysis of the nematode-trapping fungus Duddingtonia flagrans reveals high pathogenicity during nematode infection

Cited by 8 publications

References 68 publications

The Genomes of Nematode-Trapping Fungi Provide Insights into the Origin and Diversification of Fungal Carnivorism

The Genomes of Nematode-Trapping Fungi Provide Insights into the Origin and Diversification of Fungal Carnivorism

Individual and Combined Application of Nematophagous Fungi as Biological Control Agents against Gastrointestinal Nematodes in Domestic Animals

cAMP Signalling Pathway in Biocontrol Fungi

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