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Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks

BACKGROUND: Ticks are obligate bloodsucking parasites responsible for significant economic losses and concerns with human and animal health, mainly due to the transmission of pathogens. Entomopathogenic fungi have been intensively studied as an alternative strategy for tick control that can be used...

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Autores principales: Mesquita, Emily, da Costa, Diogo Paes, Meirelles, Laura Nóbrega, Camargo, Mariana Guedes, Corrêa, Thaís Almeida, Bittencourt, Vânia Rita Elias Pinheiro, da Silva Coelho, Irene, Santos, Huarrisson Azevedo, Humber, Richard Alan, Golo, Patrícia Silva
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245507/
https://www.ncbi.nlm.nih.gov/pubmed/37280668
http://dx.doi.org/10.1186/s13071-023-05790-5
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author Mesquita, Emily
da Costa, Diogo Paes
Meirelles, Laura Nóbrega
Camargo, Mariana Guedes
Corrêa, Thaís Almeida
Bittencourt, Vânia Rita Elias Pinheiro
da Silva Coelho, Irene
Santos, Huarrisson Azevedo
Humber, Richard Alan
Golo, Patrícia Silva
author_facet Mesquita, Emily
da Costa, Diogo Paes
Meirelles, Laura Nóbrega
Camargo, Mariana Guedes
Corrêa, Thaís Almeida
Bittencourt, Vânia Rita Elias Pinheiro
da Silva Coelho, Irene
Santos, Huarrisson Azevedo
Humber, Richard Alan
Golo, Patrícia Silva
author_sort Mesquita, Emily
collection PubMed
description BACKGROUND: Ticks are obligate bloodsucking parasites responsible for significant economic losses and concerns with human and animal health, mainly due to the transmission of pathogens. Entomopathogenic fungi have been intensively studied as an alternative strategy for tick control that can be used in combination with synthetic acaricides in the integrated management of ticks. Here, we investigated how the gut bacterial community of Rhipicephalus microplus is shaped after Metarhizium anisopliae treatment and how the tick susceptibility to the fungus is affected after disrupting gut bacterial microbiota. METHODS: Partially engorged tick females were artificially fed with pure bovine blood or blood plus tetracycline. Two other groups received the same diet and were topically treated with M. anisopliae. The guts were dissected, and the genomic DNA was extracted 3 days after the treatment; the V3–V4 variable region of the bacterial 16S rRNA gene was amplified. RESULTS: The gut of ticks that received no antibiotic but were treated with M. anisopliae exhibited lower bacterial diversity and a higher occurrence of Coxiella species. The Simpson diversity index and Pielou equability coefficient were higher in the gut bacterial community when R. microplus were fed with tetracycline and fungus-treated. Ticks from fungus-treated groups (with or without tetracycline) exhibited lower survival than untreated females. Previous feeding of ticks with the antibiotic did not change their susceptibility to the fungus. Ehrlichia spp. were not detected in the gueated groups. CONCLUSIONS: These findings suggest that myco-acaricidal action would not be impacted if the calf hosting these ticks is under antibiotic therapy. Moreover, the hypothesis that entomopathogenic fungi can affect the bacterial community in the gut of R. microplus engorged females is endorsed by the fact that ticks exposed to M. anisopliae exhibited a dramatic reduction in bacterial diversity. This is the first report of an entomopathogenic fungus affecting the tick gut microbiota. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05790-5.
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spelling pubmed-102455072023-06-08 Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks Mesquita, Emily da Costa, Diogo Paes Meirelles, Laura Nóbrega Camargo, Mariana Guedes Corrêa, Thaís Almeida Bittencourt, Vânia Rita Elias Pinheiro da Silva Coelho, Irene Santos, Huarrisson Azevedo Humber, Richard Alan Golo, Patrícia Silva Parasit Vectors Research BACKGROUND: Ticks are obligate bloodsucking parasites responsible for significant economic losses and concerns with human and animal health, mainly due to the transmission of pathogens. Entomopathogenic fungi have been intensively studied as an alternative strategy for tick control that can be used in combination with synthetic acaricides in the integrated management of ticks. Here, we investigated how the gut bacterial community of Rhipicephalus microplus is shaped after Metarhizium anisopliae treatment and how the tick susceptibility to the fungus is affected after disrupting gut bacterial microbiota. METHODS: Partially engorged tick females were artificially fed with pure bovine blood or blood plus tetracycline. Two other groups received the same diet and were topically treated with M. anisopliae. The guts were dissected, and the genomic DNA was extracted 3 days after the treatment; the V3–V4 variable region of the bacterial 16S rRNA gene was amplified. RESULTS: The gut of ticks that received no antibiotic but were treated with M. anisopliae exhibited lower bacterial diversity and a higher occurrence of Coxiella species. The Simpson diversity index and Pielou equability coefficient were higher in the gut bacterial community when R. microplus were fed with tetracycline and fungus-treated. Ticks from fungus-treated groups (with or without tetracycline) exhibited lower survival than untreated females. Previous feeding of ticks with the antibiotic did not change their susceptibility to the fungus. Ehrlichia spp. were not detected in the gueated groups. CONCLUSIONS: These findings suggest that myco-acaricidal action would not be impacted if the calf hosting these ticks is under antibiotic therapy. Moreover, the hypothesis that entomopathogenic fungi can affect the bacterial community in the gut of R. microplus engorged females is endorsed by the fact that ticks exposed to M. anisopliae exhibited a dramatic reduction in bacterial diversity. This is the first report of an entomopathogenic fungus affecting the tick gut microbiota. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05790-5. BioMed Central 2023-06-06 /pmc/articles/PMC10245507/ /pubmed/37280668 http://dx.doi.org/10.1186/s13071-023-05790-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Mesquita, Emily
da Costa, Diogo Paes
Meirelles, Laura Nóbrega
Camargo, Mariana Guedes
Corrêa, Thaís Almeida
Bittencourt, Vânia Rita Elias Pinheiro
da Silva Coelho, Irene
Santos, Huarrisson Azevedo
Humber, Richard Alan
Golo, Patrícia Silva
Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title_full Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title_fullStr Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title_full_unstemmed Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title_short Entomopathogenic fungus treatment changes the gut bacterial diversity of Rhipicephalus microplus ticks
title_sort entomopathogenic fungus treatment changes the gut bacterial diversity of rhipicephalus microplus ticks
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245507/
https://www.ncbi.nlm.nih.gov/pubmed/37280668
http://dx.doi.org/10.1186/s13071-023-05790-5
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