Abstract

BackgroundOphiocordyceps unilateralis is an outstanding insect fungus for its biology to manipulate host ants’ behavior and for its extreme host-specificity. Through the sequencing and annotation of Ophiocordyceps polyrhachis-furcata, a species in the O. unilateralis species complex specific to the ant Polyrhachis furcata, comparative analyses on genes involved in pathogenicity and virulence between this fungus and other fungi were undertaken in order to gain insights into its biology and the emergence of host specificity.ResultsO. polyrhachis-furcata possesses various genes implicated in pathogenicity and virulence common with other fungi. Overall, this fungus possesses protein-coding genes similar to those found on other insect fungi with available genomic resources (Beauveria bassiana, Metarhizium robertsii (formerly classified as M. anisopliae s.l.), Metarhizium acridum, Cordyceps militaris, Ophiocordyceps sinensis). Comparative analyses in regard of the host ranges of insect fungi showed a tendency toward contractions of various gene families for narrow host-range species, including cuticle-degrading genes (proteases, carbohydrate esterases) and some families of pathogen-host interaction (PHI) genes. For many families of genes, O. polyrhachis-furcata had the least number of genes found; some genes commonly found in other insect fungi are even absent (e.g. Class 1 hydrophobin). However, there are expansions of genes involved in 1) the production of bacterial-like toxins in O. polyrhachis-furcata, compared with other entomopathogenic fungi, and 2) retrotransposable elements.ConclusionsThe gain and loss of gene families helps us understand how fungal pathogenicity in insect hosts evolved. The loss of various genes involved throughout the pathogenesis for O. unilateralis would result in a reduced capacity to exploit larger ranges of hosts and therefore in the different level of host specificity, while the expansions of other gene families suggest an adaptation to particular environments with unexpected strategies like oral toxicity, through the production of bacterial-like toxins, or sophisticated mechanisms underlying pathogenicity through retrotransposons.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2101-4) contains supplementary material, which is available to authorized users.

Highlights

  • Ophiocordyceps unilateralis is an outstanding insect fungus for its biology to manipulate host ants’ behavior and for its extreme host-specificity

  • Through comparative genomics between our fungus and nineteen other fungi including other entomopathogenic fungi (B. bassiana, M. robertsii, M. acridum, C. militaris, O. sinensis), some fungal plant pathogens (Magnaporthe oryzae, Botryotinia fuckeliana, Fusarium graminearum, Sclerotinia sclerotiorum, Ustilago maydis, Verticillium alfalfae), opportunistic human pathogenic fungi and yeast (Aspergillus fumigatus, Candida albicans, Saccharomyces cerevisiae), a fungal pathogen of amphibian (Batrachochytrium dendrobatidis) and saprophytic fungi (Aspergillus nidulans, Neurospora crassa, Coprinopsis cinerea) as well as a non-pathogenic yeast (Schizosaccharomyces pombe); we identified genes involved in various steps of pathogenesis, investigated the common attributes of being entomopathogenic and the extent to which the host ranges have shaped their evolution as well as enable the discovery of new biosynthetic pathways

  • A DNA library of 3 kb, 6 kb, and 8 kb inserts were constructed and sent to Macrogen (Seoul, Republic of Korea) for sequencing on Hiseq2000 platform (Illumina). 4419 contigs together with the matepair libraries were assembled into 418 scaffolds (59 scaffolds > 1 kb; N50 3.3 Mb) with a total estimated genome size of about 43 Mb

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Summary

Introduction

Ophiocordyceps unilateralis is an outstanding insect fungus for its biology to manipulate host ants’ behavior and for its extreme host-specificity. Fungi constitute one of the most diverse kingdoms of living organisms including various forms and ecological roles such as decomposers, mutualists or parasitical symbionts Their importance for industrial and agricultural applications and their experimental tractability made them useful and popular model for studying cell biology and functional genomics in various biological context. In this regard, the number of whole-genome sequence data from a wide variety of fungi has dramatically increased during the last decade [1]. (including M. robertsii) and B. bassiana s.l., which are widely used as agents for biological control have instigated the development of genomic resources and experimental approaches in order to study virulence and pathogenicity [2, 3]. Insect fungi are well known for the production of interesting secondary metabolites such as polyketides and non-ribosomal peptides whereas the synthetic pathways have not yet been all elucidated [6]

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