Insights into adaptations to a near-obligate nematode endoparasitic lifestyle from the finished genome of Drechmeria coniospora

Authors: ZHANG, LIWEN - Chinese Academy Of Agricultural Sciences; ZHOU, ZHENGFU - Ministry Of Agriculture - China; GUO, QIANNAN - Chinese Academy Of Agricultural Sciences; FOKKENS, LIKE - University Of Amsterdam; MISKEI, MARTON - University Of Debrecen; POCSI, ISTVAN - University Of Debrecen; ZHANG, WEI - Chinese Academy Of Agricultural Sciences; CHEN, MING - Chinese Academy Of Agricultural Sciences; WANG, LEI - Nankai University; SUN, YAMIN - Nankai University; DONZELLI, BRUNO - Cornell University; GIBSON, DONNA - Former ARS Employee; NELSON, DAVID - University Of Tennessee; LUO, JIAN-GUANG - China Pharmaceutical University; REP, MARTIJN - University Of Amsterdam; HANG, LIU - Ministry Of Agriculture - China; YANG, SHENGNAN - Ministry Of Agriculture - China; WANG, JING - Ministry Of Agriculture - China; Krasnoff, Stuart; XU, YUQUAN - Ministry Of Agriculture - China; MOLNAR, ISTVAN - University Of Arizona; LIN, MIN - Chinese Academy Of Agricultural Sciences

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/29/2016
Publication Date: 3/15/2016
Citation: Zhang, L., Zhou, Z., Guo, Q., Fokkens, L., Miskei, M., Pocsi, I., Zhang, W., Chen, M., Wang, L., Sun, Y., Donzelli, B., Gibson, D.M., Nelson, D.R., Luo, J., Rep, M., Hang, L., Yang, S., Wang, J., Krasnoff, S., Xu, Y., Molnar, I., Lin, M. 2016. Insights into adaptations to a near-obligate nematode endoparasitic lifestyle from the finished genome of Drechmeria coniospora. Scientific Reports. DOI: 10.1038/srep23122.

Interpretive Summary: Drechmeria coniospora (DC) is a highly specialized fungal pathogen that attacks plant-pathogenic nematodes and lives out most of its life cycle as a parasite of nematodes. It is critical to deepen our understanding of the basic biology of this fungus to provide a knowledge base for developing it as an environmentally friendly biological control agent against economically injurious nematodes. To further this end the DC genome was sequenced and the likely functions of its genes have been identified. Analysis of the genome and comparisons with other fungal pathogens reveal that although DC has reduced the number of genes related to the ability to subsist on soil detritus (i.e. dead plant and animal material) it shares most of the genes that are responsible for successfully parasitizing its host, most notably genes coding for proteins required for attachment to and penetration of the host. Also identified were genes responsible for the biosynthesis of a potent antifungal, antibacterial, and nematicidal toxin involved in the interaction with the nematode host. The chemical structure of this toxin was elucidated so it can be studied for possible control of injurious plant pests and diseases.

Technical Abstract: Nematophagous fungi employ three distinct predatory strategies: nematode trapping, parasitism of females and eggs, and endoparasitism. While endoparasites play key roles in controlling nematode populations in nature, their application for integrated pest management is hindered by the limited understanding of their biology. We present a comparative analysis of a high quality finished genome assembly of Drechmeria coniospora, a model endoparasitic nematophagous fungus, integrated with a transcriptomic study. Adaptation of D. coniospora to its almost completely obligate endoparasitic lifestyle led to the simplification of many orthologous gene families involved in the saprophytic trophic mode, while maintaining orthologs of most known fungal pathogen-host interaction proteins, stress response circuits and putative effectors of the small secreted protein type. The need to adhere to and penetrate the host cuticle led to a selective radiation of surface proteins and hydrolytic enzymes. Although the endoparasite has a simplified secondary metabolome, it produces a novel peptaibiotic family that shows antibacterial, antifungal and nematicidal activities. Our analyses emphasize the basic malleability of the D. coniospora genome: loss of genes advantageous for the saprophytic lifestyle; modulation of elements that its cohort species utilize for entomopathogenesis; and expansion of protein families necessary for the nematode endoparasitic lifestyle.