Article

Origin and evolution of carnivorism in the Ascomycota (fungi)

State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 07/2012; 109(27):10960-10965. DOI: 10.1073/pnas.1120915109

ABSTRACT Carnivorism is one of the basic life strategies of fungi. Carnivorous fungi possess the ability to trap and digest their preys
by sophisticated trapping devices. However, the origin and development of fungal carnivorism remains a gap in evolution biology.
In this study, five protein-encoding genes were used to construct the phylogeny of the carnivorous fungi in the phylum Ascomycota;
these fungi prey on nematodes by means of specialized trapping structures such as constricting rings and adhesive traps. Our
analysis revealed a definitive pattern of evolutionary development for these trapping structures. Molecular clock calibration
based on two fossil records revealed that fungal carnivorism diverged from saprophytism about 419 Mya, which was after the
origin of nematodes about 550–600 Mya. Active carnivorism (fungi with constricting rings) and passive carnivorism (fungi with
adhesive traps) diverged from each other around 246 Mya, shortly after the occurrence of the Permian–Triassic extinction event
about 251.4 Mya. The major adhesive traps evolved around 198–208 Mya, which was within the time frame of the Triassic–Jurassic
extinction event about 201.4 Mya. However, no major carnivorous ascomycetes divergence was correlated to the Cretaceous–Tertiary
extinction event, which occurred more recently (about 65.5 Mya). Therefore, a causal relationship between mass extinction
events and fungal carnivorism evolution is not validated in this study. More evidence including additional fossil records
is needed to establish if fungal carnivorism evolution was a response to mass extinction events.

0 Bookmarks
 · 
231 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Nematode-trapping fungi are a unique group of organisms that can capture nematodes using sophisticated trapping structures. The genome of Drechslerella stenobrocha, a constricting-ring-forming fungus, has been sequenced and reported, and provided new insights into the evolutionary origins of nematode predation in fungi, the trapping mechanisms, and the dual lifestyles of saprophagy and predation. The genome of the fungus Drechslerella stenobrocha, which mechanically traps nematodes using a constricting ring, was sequenced. The genome was 29.02 Mb in size and was found rare instances of transposons and repeat induced point mutations, than that of Arthrobotrys oligospora. The functional proteins involved in nematode-infection, such as chitinases, subtilisins, and adhesive proteins, underwent a significant expansion in the A. oligospora genome, while there were fewer lectin genes that mediate fungus-nematode recognition in the D. stenobrocha genome. The carbohydrate-degrading enzyme catalogs in both species were similar to those of efficient cellulolytic fungi, suggesting a saprophytic origin of nematode-trapping fungi. In D. stenobrocha, the down-regulation of saprophytic enzyme genes and the up-regulation of infection-related genes during the capture of nematodes indicated a transition between dual life strategies of saprophagy and predation. The transcriptional profiles also indicated that trap formation was related to the protein kinase C (PKC) signal pathway and regulated by Zn(2)-C6 type transcription factors. The genome of D. stenobrocha provides support for the hypothesis that nematode trapping fungi evolved from saprophytic fungi in a high carbon and low nitrogen environment. It reveals the transition between saprophagy and predation of these fungi and also proves new insights into the mechanisms of mechanical trapping.
    BMC Genomics 02/2014; 15(1):114. · 4.40 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Malate synthase (Mls), a key enzyme in the glyoxylate cycle, is required for virulence in microbial pathogens. In this study, we identified the AoMls gene from the nematode-trapping fungus Arthobotrys oligospora. The gene contains 4 introns and encodes a polypeptide of 540 amino acids. To characterize the function of AoMls in A. oligospora, we disrupted it by homologous recombination, and the ΔAoMls mutants were confirmed by PCR and Southern blot analyses. The growth rate and colony morphology of the ΔAoMls mutants showed no obvious difference from the wild-type strains on potato dextrose agar (PDA) plate. However, the disruption of gene AoMls led to a significant reduction in conidiation, failure to utilize fatty acids and sodium acetate for growth, and its conidia were unable to germinate on minimal medium supplemented with sodium oleate. In addition, the trap formation was retarded in the ΔAoMls mutants, which only produced immature traps containing one or two rings. Moreover, the nematicidal activity of the ΔAoMls mutants was significantly decreased. Our results suggest that the gene AoMls plays an important role in conidiation, trap formation and pathogenicity of A. oligospora.
    Applied Microbiology and Biotechnology 12/2013; · 3.81 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Hirsutella minnesotensis [Ophiocordycipitaceae (Hypocreales, Ascomycota)] is a dominant endoparasitic fungus by using conidia that adhere to and penetrate the secondary stage juveniles of soybean cyst nematode (SCN). Its genome was de novo sequenced and compared with five entomopathogenic fungi in the Hypocreales and three nematode-trapping fungi in the Orbiliales (Ascomycota). The genome of H. minnesotensis is 51.4 Mb and encodes 12,702 genes enriched with transposable elements (TEs) up to 32%. Phylogenomic analysis revealed that H. minnesotensis was diverged from entomopathogenic fungi in Hypocreales. Genome of H. minnesotensis is similar to those of entomopathogenic fungi to have fewer genes encoding lectins for adhesion and glycoside hydrolases for cellulose degradation, but is different from those of nematode-trapping fungi to possess more genes for protein degradation, signal transduction and secondary metabolism. Those results indicate that H. minnesotensis has evolved different mechanism for nematode endoparasitism compared to nematode-trapping fungi. Transcriptomics analyses for the time-scale parasitism revealed the up regulations of lectins, secreted proteases and the genes for biosynthesis of secondary metabolites that could be putatively involved in host surface adhesion, cuticle degradation and host manipulation. Genome and transcriptome analyses provided comprehensive understanding of the evolution and lifestyle of nematode endoparasitism.
    Genome Biology and Evolution 10/2014; · 4.76 Impact Factor

Full-text (2 Sources)

Download
68 Downloads
Available from
May 21, 2014