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Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes.

ABSTRACT: Obligate intracellular pathogens depend on their host for growth yet must also evade detection by host defenses. Here we investigate host adaptation in two Microsporidia, the specialist Edhazardia aedis and the generalist Vavraia culicis, pathogens of disease vector mosquitoes. Genomic analysis and deep RNA-Seq across infection time courses reveal fundamental differences between these pathogens. E. aedis retains enhanced cell surface modification and signalling capacity, upregulating protein trafficking and secretion dynamically during infection. V. culicis is less dependent on its host for basic metabolites and retains a subset of spliceosomal components, with a transcriptome broadly focused on growth and replication. Transcriptional profiling of mosquito immune responses reveals that response to infection by E. aedis differs dramatically depending on the mode of infection, and that antimicrobial defensins may play a general role in mosquito defense against Microsporidia. This analysis illuminates fundamentally different evolutionary paths and host interplay of specialist and generalist pathogens.

SUBMITTER: Desjardins CA

PROVIDER: S-EPMC4435813 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes.

Desjardins Christopher A CA Sanscrainte Neil D ND Goldberg Jonathan M JM Heiman David D Young Sarah S Zeng Qiandong Q Madhani Hiten D HD Becnel James J JJ Cuomo Christina A CA

Nature communications 20150513

Obligate intracellular pathogens depend on their host for growth yet must also evade detection by host defenses. Here we investigate host adaptation in two Microsporidia, the specialist Edhazardia aedis and the generalist Vavraia culicis, pathogens of disease vector mosquitoes. Genomic analysis and deep RNA-Seq across infection time courses reveal fundamental differences between these pathogens. E. aedis retains enhanced cell surface modification and signalling capacity, upregulating protein tra ...[more]

PMID: 25968466

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Project description:Metarhizium is a genus of endophytic, insect-pathogenic fungi that is used as a biological control agent. The dual lifestyles of these fungi combine the parasitism of insect pests with the symbiotic association with plant roots. A major class of secreted metabolites by Metarhizium are cyclic depsipeptides called destruxins (DTXs). As prominent insecticidal compounds, their role during plant interactions is still largely unknown. Here, we examined the metabolomic profile of Metarhizium, with special emphasis on DTX production, using untargeted, liquid chromatography-tandem mass spectrometry (LC-MS/MS). Four Metarhizium species, two insect generalists (M. robertsii and M. brunneum), and two insect specialists (M. flavoviride and M. acridum) were inoculated onto agar plate cultures containing either bean (Phaseolus vulgaris) or corn (Zea mays) and grown for four and seven days. After methanol extraction, feature-based molecular networking (FBMN) was used to obtain DTX identification as defined by the Global Natural Products Social Molecular Networking (GNPS). A total of 25 DTX analogs were identified, with several DTX-like compounds in coculture that could not be identified. Metarhizium species differed in the amount and type of DTXs they produced, with the insect specialists producing far fewer amounts and types of DTXs than the insect generalists. The production of these metabolites varied between cultures of different ages and plant hosts. Conditions that influence the production of DTXs are discussed. As the genetic arsenal of natural products relates to the lifestyle of the organism, uncovering conditions with an ecological context may reveal strategies for producing novel compounds or precursors suitable for synthetic biology. IMPORTANCE The development of an intimate and beneficial association between fungi and plants requires an exchange of a complex mixture of chemical cues. These compounds are a means of communication, promoting or limiting the interaction, but can have numerous other biological and ecological functions. Determining how the metabolome, or a subset thereof, is linked to plant host preference and colonization has implications for future functional studies and may uncover novel therapeutic compounds whose production is elicited only under cocultivation. In this study, we performed an untargeted metabolomic analysis of plate cocultures with individual plant-fungal pairs. The identification of a major group of fungal metabolites, the destruxins, was examined for their role in plant specificity. The diversity of these metabolites and the production of numerous unidentified, structural analogs are evidence of the sensitivity of the methodology and the potential for future mining of this living data set.

Dataset Information

Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes.

Publications

Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes.

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