A genomic analysis and transcriptomic atlas of gene expression in Psoroptes ovis reveals feeding- and stage-specific patterns of allergen expression

Stewart T G Burgess,Jackie Dunn,Francesca G Nunn,Edward J Marr,Yves Van De Peer,Thomas Van Leeuwen,Alasdair J Nisbet,Kathryn Bartley,Rachel E Down,Stephane Rombauts,Jessica C Prickett,Robert J Weaver

doi:10.1186/s12864-019-6082-6

Abstract

BackgroundPsoroptic mange, caused by infestation with the ectoparasitic mite, Psoroptes ovis, is highly contagious, resulting in intense pruritus and represents a major welfare and economic concern for the livestock industry Worldwide. Control relies on injectable endectocides and organophosphate dips, but concerns over residues, environmental contamination, and the development of resistance threaten the sustainability of this approach, highlighting interest in alternative control methods. However, development of vaccines and identification of chemotherapeutic targets is hampered by the lack of P. ovis transcriptomic and genomic resources.ResultsBuilding on the recent publication of the P. ovis draft genome, here we present a genomic analysis and transcriptomic atlas of gene expression in P. ovis revealing feeding- and stage-specific patterns of gene expression, including novel multigene families and allergens. Network-based clustering revealed 14 gene clusters demonstrating either single- or multi-stage specific gene expression patterns, with 3075 female-specific, 890 male-specific and 112, 217 and 526 transcripts showing larval, protonymph and tritonymph specific-expression, respectively. Detailed analysis of P. ovis allergens revealed stage-specific patterns of allergen gene expression, many of which were also enriched in “fed” mites and tritonymphs, highlighting an important feeding-related allergenicity in this developmental stage. Pair-wise analysis of differential expression between life-cycle stages identified patterns of sex-biased gene expression and also identified novel P. ovis multigene families including known allergens and novel genes with high levels of stage-specific expression.ConclusionsThe genomic and transcriptomic atlas described here represents a unique resource for the acarid-research community, whilst the OrcAE platform makes this freely available, facilitating further community-led curation of the draft P. ovis genome.

Highlights

Psoroptic mange, caused by infestation with the ectoparasitic mite, Psoroptes ovis, is highly contagious, resulting in intense pruritus and represents a major welfare and economic concern for the livestock industry Worldwide
Functional annotation of the P. ovis predicted transcriptome derived from the draft genome Overall, 12,041 predicted protein coding genes were identified in the P. ovis genome, which represented the first global survey of the P. ovis gene repertoire [18]
The analysis showed clear patterns of gene expression attributed to individual P. ovis life cycle stages including, for the first time, the demonstration that previously-characterised allergens may exhibit both stagespecific and feeding-related patterns of gene expression; a finding of particular importance when developing novel means of control, i.e. vaccination

Summary

Introduction

Psoroptic mange, caused by infestation with the ectoparasitic mite, Psoroptes ovis, is highly contagious, resulting in intense pruritus and represents a major welfare and economic concern for the livestock industry Worldwide. Psoroptic mange, caused by the ectoparasitic mite Psoroptes ovis, is characterised by pruritus and skin irritation and is a major welfare and economic concern for the livestock industry as the parasite infests both cattle and sheep, causing the disease “sheep scab” in the latter [1, 2]. The development of novel interventions (including vaccines and the identification of potential chemotherapeutic targets) has previously been hampered by a lack of detailed transcriptomic and genomic resources for P. ovis. The integration of newly-available transcriptomic and genomic data with current knowledge of the basic biology of the mite is pivotal in the development of such novel interventions: The basic biology of the obligate ectoparasitic mite, P. ovis, on sheep is well understood, with the lifecycle taking place entirely on the ovine host and lasting from 11 to 19 days from egg hatch to egg production by the adult [5]. The role of the different developmental stages of P. ovis in eliciting the pathology associated with the host pro-inflammatory response, and subsequent semiprotective immunity, is currently unknown and would be greatly improved with knowledge of the individual life-cycle stage transcriptomes

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Conclusion