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.

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    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.
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