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: 9.67). 07/2012; 109(27):10960-10965. DOI: 10.1073/pnas.1120915109


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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Available from: Zhiqiang An, Oct 07, 2015
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    • "Nematode-trapping fungi produce sophisticated trapping structures including, one type of active mechanical trap known as constricting rings and five types of passive adhesive traps: sessile adhesive knobs, stalked knobs, adhesive nets, adhesive columns and non constricting rings. Nonconstricting rings are always associated with the stalked adhesive knobs (Yang et al., 2012). Trap cells are different from the vegetative hyphae because of the presence of numerous cytosolic organelles called dense bodies and presence of a fibrillar layer of extracellular polymers, which are believed to be important for attachment of the trap cell to the nematode surface (Andersson et al., 2013). "
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    ABSTRACT: Carnivorism is the ability of nematode-trapping fungi to trap and digest the nematodes by sophisticated devices called traps. Delivery of nematode-trapping fungi in soil for bio-control of pest nematodes often fails or gives inconsistent results. Possible reasons for failure could be the effect of soil fungistasis on germination of nematode-trapping fungi in soil environment, use of avirulent species and sensitivity of these fungi to fungicidal residues in soil. Exploitation of nematode-trapping fungi for nematode control demands that it be compatible with fungicides applied in soil or crops and proliferate in soil. This investigation represents is one of the first to evaluate the effect of fungicides on the nematode-trapping fungus Arthrobotrys dactyloides. A. dactyloides showed in vitro carnivorous potential against Meloidogyne incognita, Meloidogyne javanica, Meloidogyne graminicola, Helicotylenchus dihystera and Heterodera cajani. Conidia of A. dactyloides exposed to agricultural soils showed poor germination but formed conidial traps, which captured and killed the soil nematodes. Conidial traps, which trapped the nematodes, grew well in all soils after killing and nutrient absorption from nematode body. Soil amended with 20 mg ai kg−1 of carbendazim and thiram, 30 mg ai kg−1 of mancozeb, 50 mg ai kg−1 of captan, and 100 mg ai kg−1 of carboxin completely checked the conidial trap formation and nematode capturing. 30, 50 and 100 mg ai kg−1 of metalaxyl adversely affected the conidial trap formation and nematode capturing in soil. Propiconazole inhibited 15.2% conidial trap formation up to 50 mg ai kg−1 but caused 93.3% inhibition of conidial traps formation and complete inhibition of nematode capturing at 100 mg ai kg−1. Sulphur, triademefon, and tricyclazole showed least toxic effect on conidial trap formation and nematode capturing activities of A. dactyloides in soil up to 100 mg ai kg−1.
    Biological Control 03/2015; 82. DOI:10.1016/j.biocontrol.2014.12.014 · 1.64 Impact Factor
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    • "Some wood-decaying fungi may have evolved to capture tiny animals for nitrogen under this environmental selection pressure [11]. A phylogenetic analysis based on the conservative genes of nematode-trapping fungi belonging to Ascomycetes also suggests a possible causal relationship between mass extinction events and the evolution of fungal predation [9]. Predatory fungi gained a competitive advantage over strict saprobes by predating tiny animals when available organic matter decreased during the ecosystem recovery [9]. "
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    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. DOI:10.1186/1471-2164-15-114 · 3.99 Impact Factor
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    ABSTRACT: Nematophagous fungi can trap and capture nematodes and other small invertebrates. This unique ability has made them ideal organisms from which to develop biological control agents against plant- and animal-parasitic nematodes. However, effective application of biocontrol agents in the field requires a comprehensive understanding about the ecology and population genetics of the nematophagous fungi in natural environments. Here, we genotyped 228 strains of the nematode-trapping fungus using 12 single nucleotide polymorphic markers located on eight random DNA fragments. The strains were from different ecological niches and geographical regions from China. Our analyses identified that ecological niche separations contributed significantly, whereas geographic separation contributed relatively little to the overall genetic variation in our samples of . Interestingly, populations from stressful environments seemed to be more variable and showed more evidence for recombination than those from benign environments at the same geographic areas. We discussed the implications of our results to the conservation and biocontrol application of in agriculture and forestry.
    Ecology and Evolution 02/2013; 3(2). DOI:10.1002/ece3.450 · 2.32 Impact Factor
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