Comparative Genomics and Transcriptomics Analyses Reveal Divergent Lifestyle Features of Nematode Endoparasitic Fungus Hirsutella minnesotensis

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. 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 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 with nematode-trapping fungi. Transcriptomics analyses for the time-scale parasitism revealed the upregulations 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.

Introgression and gene family contraction drive the evolution of lifestyle and host shifts of hypocrealean fungi

“…The nematode endoparasitic Hirsutella spp. and ghost moths parasite O. sinensis are both host density-dependent obligate pathogens, indicated their strong interactions with and dependence upon their hosts (Hu et al 2013; Lai et al 2014). The large number of TEs in the genomes of these fungi might be associated with their obligate interactions with their hosts.

10.1080/21501203.2018.1478333-F0002Figure 2.Average genome sizes, gene numbers and gene densities of fungal lineages employing different life strategies.(A) Left axis shows genome sizes (Mb) and right axis shows gene numbers.

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“…Generally, genomic analysis revealed that a higher abundance of CAZymes is associated with the utilisation of plant-based nutrition, while greater numbers of proteases and chitinases are associated with insect-based nutrition, while only proteases are associated with nematode-based nutrition (Dimitrios et al 2012; Xiao et al 2012; Lai et al 2014; Liu et al 2014). A series of CAZymes involved in carbohydrate degradation were significantly contracted during the lifestyle transition from plant pathogens to other animal pathogenic, mycoparasitic or endophytic lifestyles.…”

Population Genetics of Hirsutella rhossiliensis, a Dominant Parasite of Cyst Nematode Juveniles on a Continental Scale

“…However, the number of phylogenetically informative sites provided by the three fragments was insufficient. Therefore, novel DNA markers were determined by searching the genome data (15). Specifically, 27 fragments of genes putatively involved in the infection processes of H. rhossiliensis into nematodes and 15 fragments of interest as a result of a genomic comparison between H. minnesotensis and H. rhossiliensis were chosen as candidate markers.…”

“…In the agricultural fields, the plants, nematodes, and endoparasitic fungi constitute a tight tripartite system with the plants providing food to nematodes and the nematodes serving as nitrogen sources to endoparasitic fungi. This existing natural interaction suggests that endoparasitic fungi could have great potential for use as biocontrol agents to control nematodes in a sustainable manner (13)(14)(15).…”

Characterization of a new toxin from the entomopathogenic fungus Metarhizium anisopliae: the ribotoxin anisoplin

“…Moreover, efficient compartmentalization and secretion by the producer fungus seems to be the best self-defense mechanism against endogenous ribotoxin production (Endo et al, 1993a;Martínez-Ruiz et al, 1998), so signal peptide in anisoplin might have evolved in this sense. From an evolutionary point of view, the entomopathogens Metarhizium and Hirsutella are closer in the phylogenetic tree than Aspergillus (Lai et al, 2014). It is not surprising then that anisoplin better resembles HtA than any other known ribotoxin.…”