De novo transcriptome sequencing of the northern fowl mite, Ornithonyssus sylviarum, shed light on parasitiform poultry mites evolution and its chemoreceptor repertoires

Bhowmick, Biswajit; Chen, Huaqing; Lozano-Fernandez, Jesus; Vizueta, Joel; Ignell, Rickard; Han, Qian

doi:10.1007/s00436-022-07432-8

Arthropods and Medical Entomology - Original Paper
Published: 15 January 2022

De novo transcriptome sequencing of the northern fowl mite, Ornithonyssus sylviarum, shed light on parasitiform poultry mites evolution and its chemoreceptor repertoires

Biswajit Bhowmick^1,2,
Huaqing Chen^1,2,
Jesus Lozano-Fernandez^3,4,
Joel Vizueta⁵,
Rickard Ignell⁶ &
Qian Han ORCID: orcid.org/0000-0001-6245-5252^1,2

Parasitology Research volume 121, pages 521–535 (2022)Cite this article

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Abstract

The northern fowl mite (NFM), Ornithonyssus sylviarum, and the poultry red mite (PRM), Dermanyssus gallinae, are the most serious pests of poultry, both of which have an expanding global prevalence. Research on NFM has been constrained by a lack of genomic and transcriptomic data. Here, we report and analyze the first global transcriptome data across all mite live stages and sexes. A total of 28,999 unigenes were assembled, of which 19,750 (68.10%) were annotated using seven functional databases. The biological function of these unigenes was classified using the GO, KOG, and KEGG databases. To gain insight into the chemosensory receptor-based system of parasitiform mites, we furthermore assessed the gene repertoire of gustatory receptors (GRs) and ionotropic receptors (IRs), both of which encode putative ligand-gated ion channel proteins. While these receptors are well characterized in insect model species, our understanding of chemosensory detection in mites and ticks is in its infancy. To address this paucity of data, we identified 9 IR/iGluRs and 2 GRs genes by analyzing transcriptome data in the NFM, while 9 GRs and 41 IR/iGluRs genes were annotated in the PRM genome. Taken together, the transcriptomic and genomic annotation of these two species provide a valuable reference for studies of parasitiform mites and also help to understand how chemosensory gene family expansion/contraction events may have been reshaped by an obligate parasitic lifestyle compared with their free-living closest relatives. Future studies should include additional species to validate this observation and functional characterization of the identified proteins as a step forward in identifying tools for controlling these poultry pests.

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Abbreviations

NFM:: Northern fowl mite
PRM:: Poultry red mite
NMDA:: N-methyl-d-aspartate
AMPA:: α-Amino-3-hydroxy-5-methyl-4-isoxazole propionate
ORCAE:: Online Resource for Community Annotation of Eukaryotes
HTS:: High-throughput sequencing

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Acknowledgements

We would like to thank Yu Tang, Dr. Jianguo Zhao, and Dr. Chenghong Liao for their assistance.

Funding

This work was supported by Hainan Provincial Major R & D Program (ZDKJ2021035).

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Authors and Affiliations

Laboratory of Tropical Veterinary Medicine and Vector Biology, School of Life and Pharmaceutical Sciences, Hainan University, Haikou, 570228, Hainan, China
Biswajit Bhowmick, Huaqing Chen & Qian Han
One Health Institute, Hainan University, Haikou, 570228, Hainan, China
Biswajit Bhowmick, Huaqing Chen & Qian Han
Institute of Evolutionary Biology (CSIC-UPF), Pg. Marítim de la Barceloneta 39-47, 08003, Barcelona, Spain
Jesus Lozano-Fernandez
Department of Genetics, Microbiology and Statistics, Biodiversity Research Institute (IRBio), University of Barcelona, Avd. Diagonal 643, 08028, Barcelona, Spain
Jesus Lozano-Fernandez
Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark
Joel Vizueta
Disease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, 23053, Alnarp, Sweden
Rickard Ignell

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Biswajit Bhowmick
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Huaqing Chen
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Jesus Lozano-Fernandez
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Joel Vizueta
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Rickard Ignell
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Qian Han
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Contributions

B.B. and Q.H. conceived and designed the study. B.B. and H.C. wrote the first draft and performed the experiments. J.L.-F., J.V., R.I., and Q.H. commented on study design, methodology, and substantially revised the manuscript. All authors approved the final version.

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Correspondence to Qian Han.

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All procedures to gather samples from animals were approved by Hainan University Institutional Animal Care and Use Committee (HNUAUCC-2019-0000A).

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Bhowmick, B., Chen, H., Lozano-Fernandez, J. et al. De novo transcriptome sequencing of the northern fowl mite, Ornithonyssus sylviarum, shed light on parasitiform poultry mites evolution and its chemoreceptor repertoires. Parasitol Res 121, 521–535 (2022). https://doi.org/10.1007/s00436-022-07432-8

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Received: 10 May 2021
Accepted: 17 December 2021
Published: 15 January 2022
Issue Date: February 2022
DOI: https://doi.org/10.1007/s00436-022-07432-8

Keywords

Chemosensory receptors
De novo assembly
Ectoparasites
Genomics
Phylogeny
Parasitiformes