Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.

Aedes aegypti is the principal mosquito vector of dengue, yellow fever, Zika and chikungunya viruses. The wMel strain of the endosymbiotic bacteria Wolbachia pipientis was introduced into the vector as a novel biocontrol strategy to stop transmission of these viruses. Mosquitoes with Wolbachia have...

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Published in:PLOS Neglected Tropical Diseases
Main Authors: B M C Randika Wimalasiri-Yapa, Bixing Huang, Perran A Ross, Ary A Hoffmann, Scott A Ritchie, Francesca D Frentiu, David Warrilow, Andrew F van den Hurk
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2023
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0011222
https://doaj.org/article/c6596d63d8e24b21b15c86dfd5806b8b
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spelling ftdoajarticles:oai:doaj.org/article:c6596d63d8e24b21b15c86dfd5806b8b 2023-06-11T04:09:56+02:00 Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia. B M C Randika Wimalasiri-Yapa Bixing Huang Perran A Ross Ary A Hoffmann Scott A Ritchie Francesca D Frentiu David Warrilow Andrew F van den Hurk 2023-03-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0011222 https://doaj.org/article/c6596d63d8e24b21b15c86dfd5806b8b EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0011222 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0011222 https://doaj.org/article/c6596d63d8e24b21b15c86dfd5806b8b PLoS Neglected Tropical Diseases, Vol 17, Iss 3, p e0011222 (2023) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2023 ftdoajarticles https://doi.org/10.1371/journal.pntd.0011222 2023-05-07T00:31:57Z Aedes aegypti is the principal mosquito vector of dengue, yellow fever, Zika and chikungunya viruses. The wMel strain of the endosymbiotic bacteria Wolbachia pipientis was introduced into the vector as a novel biocontrol strategy to stop transmission of these viruses. Mosquitoes with Wolbachia have been released in the field in Northern Queensland, Australia since 2011, at various locations and over several years, with populations remaining stably infected. Wolbachia infection is known to alter gene expression in its mosquito host, but whether (and how) this changes over the long-term in the context of field releases remains unknown. We sampled mosquitoes from Wolbachia-infected populations with three different release histories along a time gradient and performed RNA-seq to investigate gene expression changes in the insect host. We observed a significant impact on gene expression in Wolbachia-infected mosquitoes versus uninfected controls. Fewer genes had significantly upregulated expression in mosquitoes from the older releases (512 and 486 from the 2011 and 2013/14 release years, respectively) versus the more recent releases (1154 from the 2017 release year). Nonetheless, a fundamental signature of Wolbachia infection on host gene expression was observed across all releases, comprising upregulation of immunity (e.g. leucine-rich repeats, CLIPs) and metabolism (e.g. lipid metabolism, iron transport) genes. There was limited downregulation of gene expression in mosquitoes from the older releases (84 and 71 genes from the 2011 and 2013/14 release years, respectively), but significantly more in the most recent release (509 from the 2017 release year). Our findings indicate that at > 8 years post-introgression into field populations, Wolbachia continues to profoundly impact expression of host genes, such as those involved in insect immune response and metabolism. If Wolbachia-mediated virus blocking is underpinned by these differential gene expression changes, our results suggest it may remain stable long-term. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic Queensland PLOS Neglected Tropical Diseases 17 3 e0011222
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
B M C Randika Wimalasiri-Yapa
Bixing Huang
Perran A Ross
Ary A Hoffmann
Scott A Ritchie
Francesca D Frentiu
David Warrilow
Andrew F van den Hurk
Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description Aedes aegypti is the principal mosquito vector of dengue, yellow fever, Zika and chikungunya viruses. The wMel strain of the endosymbiotic bacteria Wolbachia pipientis was introduced into the vector as a novel biocontrol strategy to stop transmission of these viruses. Mosquitoes with Wolbachia have been released in the field in Northern Queensland, Australia since 2011, at various locations and over several years, with populations remaining stably infected. Wolbachia infection is known to alter gene expression in its mosquito host, but whether (and how) this changes over the long-term in the context of field releases remains unknown. We sampled mosquitoes from Wolbachia-infected populations with three different release histories along a time gradient and performed RNA-seq to investigate gene expression changes in the insect host. We observed a significant impact on gene expression in Wolbachia-infected mosquitoes versus uninfected controls. Fewer genes had significantly upregulated expression in mosquitoes from the older releases (512 and 486 from the 2011 and 2013/14 release years, respectively) versus the more recent releases (1154 from the 2017 release year). Nonetheless, a fundamental signature of Wolbachia infection on host gene expression was observed across all releases, comprising upregulation of immunity (e.g. leucine-rich repeats, CLIPs) and metabolism (e.g. lipid metabolism, iron transport) genes. There was limited downregulation of gene expression in mosquitoes from the older releases (84 and 71 genes from the 2011 and 2013/14 release years, respectively), but significantly more in the most recent release (509 from the 2017 release year). Our findings indicate that at > 8 years post-introgression into field populations, Wolbachia continues to profoundly impact expression of host genes, such as those involved in insect immune response and metabolism. If Wolbachia-mediated virus blocking is underpinned by these differential gene expression changes, our results suggest it may remain stable long-term.
format Article in Journal/Newspaper
author B M C Randika Wimalasiri-Yapa
Bixing Huang
Perran A Ross
Ary A Hoffmann
Scott A Ritchie
Francesca D Frentiu
David Warrilow
Andrew F van den Hurk
author_facet B M C Randika Wimalasiri-Yapa
Bixing Huang
Perran A Ross
Ary A Hoffmann
Scott A Ritchie
Francesca D Frentiu
David Warrilow
Andrew F van den Hurk
author_sort B M C Randika Wimalasiri-Yapa
title Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
title_short Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
title_full Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
title_fullStr Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
title_full_unstemmed Differences in gene expression in field populations of Wolbachia-infected Aedes aegypti mosquitoes with varying release histories in northern Australia.
title_sort differences in gene expression in field populations of wolbachia-infected aedes aegypti mosquitoes with varying release histories in northern australia.
publisher Public Library of Science (PLoS)
publishDate 2023
url https://doi.org/10.1371/journal.pntd.0011222
https://doaj.org/article/c6596d63d8e24b21b15c86dfd5806b8b
geographic Arctic
Queensland
geographic_facet Arctic
Queensland
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 17, Iss 3, p e0011222 (2023)
op_relation https://doi.org/10.1371/journal.pntd.0011222
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0011222
https://doaj.org/article/c6596d63d8e24b21b15c86dfd5806b8b
op_doi https://doi.org/10.1371/journal.pntd.0011222
container_title PLOS Neglected Tropical Diseases
container_volume 17
container_issue 3
container_start_page e0011222
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