Cargando…

Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle

BACKGROUND: The blood feeding poultry red mite (PRM), Dermanyssus gallinae, causes substantial economic damage to the egg laying industry worldwide, and is a serious welfare concern for laying hens and poultry house workers. In this study we have investigated the temporal gene expression across the...

Descripción completa

Detalles Bibliográficos
Autores principales: Bartley, Kathryn, Chen, Wan, Lloyd Mills, Richard I., Nunn, Francesca, Price, Daniel R. G., Rombauts, Stephane, Van de Peer, Yves, Roy, Lise, Nisbet, Alasdair J., Burgess, Stewart T. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8028124/
https://www.ncbi.nlm.nih.gov/pubmed/33827430
http://dx.doi.org/10.1186/s12864-021-07547-9
_version_ 1783675926461022208
author Bartley, Kathryn
Chen, Wan
Lloyd Mills, Richard I.
Nunn, Francesca
Price, Daniel R. G.
Rombauts, Stephane
Van de Peer, Yves
Roy, Lise
Nisbet, Alasdair J.
Burgess, Stewart T. G.
author_facet Bartley, Kathryn
Chen, Wan
Lloyd Mills, Richard I.
Nunn, Francesca
Price, Daniel R. G.
Rombauts, Stephane
Van de Peer, Yves
Roy, Lise
Nisbet, Alasdair J.
Burgess, Stewart T. G.
author_sort Bartley, Kathryn
collection PubMed
description BACKGROUND: The blood feeding poultry red mite (PRM), Dermanyssus gallinae, causes substantial economic damage to the egg laying industry worldwide, and is a serious welfare concern for laying hens and poultry house workers. In this study we have investigated the temporal gene expression across the 6 stages/sexes (egg, larvae, protonymph and deutonymph, adult male and adult female) of this neglected parasite in order to understand the temporal expression associated with development, parasitic lifestyle, reproduction and allergen expression. RESULTS: RNA-seq transcript data for the 6 stages were mapped to the PRM genome creating a publicly available gene expression atlas (on the OrcAE platform in conjunction with the PRM genome). Network analysis and clustering of stage-enriched gene expression in PRM resulted in 17 superclusters with stage-specific or multi-stage expression profiles. The 6 stage specific superclusters were clearly demarked from each other and the adult female supercluster contained the most stage specific transcripts (2725), whilst the protonymph supercluster the fewest (165). Fifteen pairwise comparisons performed between the different stages resulted in a total of 6025 Differentially Expressed Genes (DEGs) (P > 0.99). These data were evaluated alongside a Venn/Euler analysis of the top 100 most abundant genes in each stage. An expanded set of cuticle proteins and enzymes (chitinase and metallocarboxypeptidases) were identified in larvae and underpin cuticle formation and ecdysis to the protonymph stage. Two mucin/peritrophic-A salivary proteins (DEGAL6771g00070, DEGAL6824g00220) were highly expressed in the blood-feeding stages, indicating peritrophic membrane formation during feeding. Reproduction-associated vitellogenins were the most abundant transcripts in adult females whilst, in adult males, an expanded set of serine and cysteine proteinases and an epididymal protein (DEGAL6668g00010) were highly abundant. Assessment of the expression patterns of putative homologues of 32 allergen groups from house dust mites indicated a bias in their expression towards the non-feeding larval stage of PRM. CONCLUSIONS: This study is the first evaluation of temporal gene expression across all stages of PRM and has provided insight into developmental, feeding, reproduction and survival strategies employed by this mite. The publicly available PRM resource on OrcAE offers a valuable tool for researchers investigating the biology and novel interventions of this parasite. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07547-9.
format Online
Article
Text
id pubmed-8028124
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-80281242021-04-08 Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle Bartley, Kathryn Chen, Wan Lloyd Mills, Richard I. Nunn, Francesca Price, Daniel R. G. Rombauts, Stephane Van de Peer, Yves Roy, Lise Nisbet, Alasdair J. Burgess, Stewart T. G. BMC Genomics Research Article BACKGROUND: The blood feeding poultry red mite (PRM), Dermanyssus gallinae, causes substantial economic damage to the egg laying industry worldwide, and is a serious welfare concern for laying hens and poultry house workers. In this study we have investigated the temporal gene expression across the 6 stages/sexes (egg, larvae, protonymph and deutonymph, adult male and adult female) of this neglected parasite in order to understand the temporal expression associated with development, parasitic lifestyle, reproduction and allergen expression. RESULTS: RNA-seq transcript data for the 6 stages were mapped to the PRM genome creating a publicly available gene expression atlas (on the OrcAE platform in conjunction with the PRM genome). Network analysis and clustering of stage-enriched gene expression in PRM resulted in 17 superclusters with stage-specific or multi-stage expression profiles. The 6 stage specific superclusters were clearly demarked from each other and the adult female supercluster contained the most stage specific transcripts (2725), whilst the protonymph supercluster the fewest (165). Fifteen pairwise comparisons performed between the different stages resulted in a total of 6025 Differentially Expressed Genes (DEGs) (P > 0.99). These data were evaluated alongside a Venn/Euler analysis of the top 100 most abundant genes in each stage. An expanded set of cuticle proteins and enzymes (chitinase and metallocarboxypeptidases) were identified in larvae and underpin cuticle formation and ecdysis to the protonymph stage. Two mucin/peritrophic-A salivary proteins (DEGAL6771g00070, DEGAL6824g00220) were highly expressed in the blood-feeding stages, indicating peritrophic membrane formation during feeding. Reproduction-associated vitellogenins were the most abundant transcripts in adult females whilst, in adult males, an expanded set of serine and cysteine proteinases and an epididymal protein (DEGAL6668g00010) were highly abundant. Assessment of the expression patterns of putative homologues of 32 allergen groups from house dust mites indicated a bias in their expression towards the non-feeding larval stage of PRM. CONCLUSIONS: This study is the first evaluation of temporal gene expression across all stages of PRM and has provided insight into developmental, feeding, reproduction and survival strategies employed by this mite. The publicly available PRM resource on OrcAE offers a valuable tool for researchers investigating the biology and novel interventions of this parasite. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07547-9. BioMed Central 2021-04-07 /pmc/articles/PMC8028124/ /pubmed/33827430 http://dx.doi.org/10.1186/s12864-021-07547-9 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Bartley, Kathryn
Chen, Wan
Lloyd Mills, Richard I.
Nunn, Francesca
Price, Daniel R. G.
Rombauts, Stephane
Van de Peer, Yves
Roy, Lise
Nisbet, Alasdair J.
Burgess, Stewart T. G.
Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title_full Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title_fullStr Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title_full_unstemmed Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title_short Transcriptomic analysis of the poultry red mite, Dermanyssus gallinae, across all stages of the lifecycle
title_sort transcriptomic analysis of the poultry red mite, dermanyssus gallinae, across all stages of the lifecycle
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8028124/
https://www.ncbi.nlm.nih.gov/pubmed/33827430
http://dx.doi.org/10.1186/s12864-021-07547-9
work_keys_str_mv AT bartleykathryn transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT chenwan transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT lloydmillsrichardi transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT nunnfrancesca transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT pricedanielrg transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT rombautsstephane transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT vandepeeryves transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT roylise transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT nisbetalasdairj transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle
AT burgessstewarttg transcriptomicanalysisofthepoultryredmitedermanyssusgallinaeacrossallstagesofthelifecycle