Genomic and Proteomic Analyses of the Fungus Arthrobotrys oligospora Provide Insights into Nematode-Trap Formation

Abstract

Nematode-trapping fungi are “carnivorous” and attack their hosts using specialized trapping devices. The morphological development of these traps is the key indicator of their switch from saprophytic to predacious lifestyles. Here, the genome of the nematode-trapping fungus Arthrobotrys oligospora Fres. (ATCC24927) was reported. The genome contains 40.07 Mb assembled sequence with 11,479 predicted genes. Comparative analysis showed that A. oligospora shared many more genes with pathogenic fungi than with non-pathogenic fungi. Specifically, compared to several sequenced ascomycete fungi, the A. oligospora genome has a larger number of pathogenicity-related genes in the subtilisin, cellulase, cellobiohydrolase, and pectinesterase gene families. Searching against the pathogen-host interaction gene database identified 398 homologous genes involved in pathogenicity in other fungi. The analysis of repetitive sequences provided evidence for repeat-induced point mutations in A. oligospora. Proteomic and quantitative PCR (qPCR) analyses revealed that 90 genes were significantly up-regulated at the early stage of trap-formation by nematode extracts and most of these genes were involved in translation, amino acid metabolism, carbohydrate metabolism, cell wall and membrane biogenesis. Based on the combined genomic, proteomic and qPCR data, a model for the formation of nematode trapping device in this fungus was proposed. In this model, multiple fungal signal transduction pathways are activated by its nematode prey to further regulate downstream genes associated with diverse cellular processes such as energy metabolism, biosynthesis of the cell wall and adhesive proteins, cell division, glycerol accumulation and peroxisome biogenesis. This study will facilitate the identification of pathogenicity-related genes and provide a broad foundation for understanding the molecular and evolutionary mechanisms underlying fungi-nematodes interactions.

Proteome of the Nematode-Trapping Cells of the Fungus Monacrosporium haptotylum

“…Previous proteome studies of nematode-trapping fungi have involved species such as Monacrosporium lysipagum and A. oligospora, where the trap cells cannot be isolated from the mycelium (10,38). Given that the biomass of trap cells is considerably lower than that of the mycelium, it is difficult to infer the trap proteome by comparing the proteomes of a mycelium with and without traps.…”

“…Indeed, in the recently published ge- nome of A. oligospora, seven lectins with different sugar specificities were identified (10). The expression levels of the mRNAs and the corresponding proteins of these lectins did not change during trap formation, and their roles in the trapping mechanism remain unclear (10). In the genome of M. haptotylum, we identified homologs of six of the seven lectins in A. oligospora.…”

“…However, deletion of the gene did not affect the ability to infect nematodes (61), which suggests that the fungus might express other lectins mediating attachment to nematodes. Indeed, in the recently published ge- nome of A. oligospora, seven lectins with different sugar specificities were identified (10). The expression levels of the mRNAs and the corresponding proteins of these lectins did not change during trap formation, and their roles in the trapping mechanism remain unclear (10).…”

“…We have recently sequenced the genome of M. haptotylum (T. Meerupati, K.-M. Andersson, E. Friman, D. Kumar, A. Tunlid, and D. Ahrén, submitted for publication) and detected many similarities to the genome of the net-forming nematode-trapping fungus Arthrobotrys oligospora (10). The two genomes are similar in size and consist of ϳ62% core genes that are shared with other fungi, ϳ20% genes that are specific to the two species, and ϳ16% genes that are unique to each genome.…”

Genomic Insights into the Adaptation to Parasitism in Nematode-Trapping Fungi and Transcriptomics during Infection of Caenorhabditis Briggsae and Plant-Parasitic Nematodes

“…To know the genomic mechanism responsible for adaptation of parasitism in nematode trapping fungi, genome of the adhesive knob forming fungus Monoacrosporium haptotylum was sequenced to 28 fold coverage using 454 pyrosequencing and compared with the available genome sequence of Arthrobotrys oligospora (Yang et al, 2011). The genome size of M. haptotylum was estimated to 40.4 Mb and protein-coding genes to 10,959 which are more or less similar to the numbers for A. oligospora (Table 1).…”