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Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)

BACKGROUND: Microsporidia are highly specialized, parasitic fungi that infect a wide range of eukaryotic hosts from all major taxa. Infections cause a variety of damaging effects on host physiology from increased stress to death. The microsporidian Facilispora margolisi infects the Pacific salmon lo...

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Autores principales: Poley, Jordan D., Sutherland, Ben J. G., Fast, Mark D., Koop, Ben F., Jones, Simon R. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5561633/
https://www.ncbi.nlm.nih.gov/pubmed/28818044
http://dx.doi.org/10.1186/s12864-017-4040-8
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author Poley, Jordan D.
Sutherland, Ben J. G.
Fast, Mark D.
Koop, Ben F.
Jones, Simon R. M.
author_facet Poley, Jordan D.
Sutherland, Ben J. G.
Fast, Mark D.
Koop, Ben F.
Jones, Simon R. M.
author_sort Poley, Jordan D.
collection PubMed
description BACKGROUND: Microsporidia are highly specialized, parasitic fungi that infect a wide range of eukaryotic hosts from all major taxa. Infections cause a variety of damaging effects on host physiology from increased stress to death. The microsporidian Facilispora margolisi infects the Pacific salmon louse (Lepeophtheirus salmonis oncorhynchi), an economically and ecologically important ectoparasitic copepod that can impact wild and cultured salmonids. RESULTS: Vertical transmission of F. margolisi was demonstrated by using PCR and in situ hybridization to identify and localize microsporidia in female L. salmonis and their offspring. Spores and developmental structures of F. margolisi were identified in 77% of F(1) generation copepods derived from infected females while offspring from uninfected females all tested negative for the microsporidia. The transcriptomic response of the salmon louse to F. margolisi was profiled at both the copepodid larval stage and the pre-adult stage using microarray technology. Infected copepodids differentially expressed 577 transcripts related to stress, ATP generation and structural components of muscle and cuticle. The infection also impacted the response of the copepodid to the parasiticide emamectin benzoate (EMB) at a low dose of 1.0 ppb for 24 h. A set of 48 transcripts putatively involved in feeding and host immunomodulation were up to 8-fold underexpressed in the F. margolisi infected copepodids treated with EMB compared with controls or either stressor alone. Additionally, these infected lice treated with EMB also overexpressed 101 transcripts involved in stress resistance and signalling compared to the other groups. In contrast, infected pre-adult lice did not display a stress response, suggesting a decrease in microsporidian virulence associated with lice maturity. Furthermore, copepodid infectivity and moulting was not affected by the microsporidian infection. CONCLUSIONS: This study demonstrated that F. margolisi is transmitted vertically between salmon louse generations and that biological impacts of infection differ depending on the stage of the copepod host. The infection caused significant perturbations of larval transcriptomes and therefore must be considered in future studies in which impacts to host development and environmental factors are assessed. Fitness impacts are probably minor, although the interaction between pesticide exposure and microsporidian infection merits further study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-4040-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-55616332017-08-18 Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis) Poley, Jordan D. Sutherland, Ben J. G. Fast, Mark D. Koop, Ben F. Jones, Simon R. M. BMC Genomics Research Article BACKGROUND: Microsporidia are highly specialized, parasitic fungi that infect a wide range of eukaryotic hosts from all major taxa. Infections cause a variety of damaging effects on host physiology from increased stress to death. The microsporidian Facilispora margolisi infects the Pacific salmon louse (Lepeophtheirus salmonis oncorhynchi), an economically and ecologically important ectoparasitic copepod that can impact wild and cultured salmonids. RESULTS: Vertical transmission of F. margolisi was demonstrated by using PCR and in situ hybridization to identify and localize microsporidia in female L. salmonis and their offspring. Spores and developmental structures of F. margolisi were identified in 77% of F(1) generation copepods derived from infected females while offspring from uninfected females all tested negative for the microsporidia. The transcriptomic response of the salmon louse to F. margolisi was profiled at both the copepodid larval stage and the pre-adult stage using microarray technology. Infected copepodids differentially expressed 577 transcripts related to stress, ATP generation and structural components of muscle and cuticle. The infection also impacted the response of the copepodid to the parasiticide emamectin benzoate (EMB) at a low dose of 1.0 ppb for 24 h. A set of 48 transcripts putatively involved in feeding and host immunomodulation were up to 8-fold underexpressed in the F. margolisi infected copepodids treated with EMB compared with controls or either stressor alone. Additionally, these infected lice treated with EMB also overexpressed 101 transcripts involved in stress resistance and signalling compared to the other groups. In contrast, infected pre-adult lice did not display a stress response, suggesting a decrease in microsporidian virulence associated with lice maturity. Furthermore, copepodid infectivity and moulting was not affected by the microsporidian infection. CONCLUSIONS: This study demonstrated that F. margolisi is transmitted vertically between salmon louse generations and that biological impacts of infection differ depending on the stage of the copepod host. The infection caused significant perturbations of larval transcriptomes and therefore must be considered in future studies in which impacts to host development and environmental factors are assessed. Fitness impacts are probably minor, although the interaction between pesticide exposure and microsporidian infection merits further study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-4040-8) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-17 /pmc/articles/PMC5561633/ /pubmed/28818044 http://dx.doi.org/10.1186/s12864-017-4040-8 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Poley, Jordan D.
Sutherland, Ben J. G.
Fast, Mark D.
Koop, Ben F.
Jones, Simon R. M.
Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title_full Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title_fullStr Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title_full_unstemmed Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title_short Effects of the vertically transmitted microsporidian Facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (Lepeophtheirus salmonis)
title_sort effects of the vertically transmitted microsporidian facilispora margolisi and the parasiticide emamectin benzoate on salmon lice (lepeophtheirus salmonis)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5561633/
https://www.ncbi.nlm.nih.gov/pubmed/28818044
http://dx.doi.org/10.1186/s12864-017-4040-8
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