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A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick

Amblyomma americanum (Lone star tick) is an important disease vector in the United States. It transmits several human pathogens, including the agents of human monocytic ehrlichiosis, tularemia, and southern tick-associated rash illness. Blood-feeding insects (Class Insecta) depend on bacterial endos...

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Autores principales: Smith, Todd A, Driscoll, Timothy, Gillespie, Joseph J, Raghavan, Rahul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994718/
https://www.ncbi.nlm.nih.gov/pubmed/25618142
http://dx.doi.org/10.1093/gbe/evv016
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author Smith, Todd A
Driscoll, Timothy
Gillespie, Joseph J
Raghavan, Rahul
author_facet Smith, Todd A
Driscoll, Timothy
Gillespie, Joseph J
Raghavan, Rahul
author_sort Smith, Todd A
collection PubMed
description Amblyomma americanum (Lone star tick) is an important disease vector in the United States. It transmits several human pathogens, including the agents of human monocytic ehrlichiosis, tularemia, and southern tick-associated rash illness. Blood-feeding insects (Class Insecta) depend on bacterial endosymbionts to provide vitamins and cofactors that are scarce in blood. It is unclear how this deficiency is compensated in ticks (Class Arachnida) that feed exclusively on mammalian blood. A bacterium related to Coxiella burnetii, the agent of human Q fever, has been observed previously within cells of A. americanum. Eliminating this bacterium (CLEAA, Coxiella-like endosymbiont of A. americanum) with antibiotics reduced tick fecundity, indicating that it is an essential endosymbiont. In an effort to determine its role within this symbiosis, we sequenced the CLEAA genome. While highly reduced (656,901 bp) compared with C. burnetii (1,995,281 bp), the CLEAA genome encodes most major vitamin and cofactor biosynthesis pathways, implicating CLEAA as a vitamin provisioning endosymbiont. In contrast, CLEAA lacks any recognizable virulence genes, indicating that it is not a pathogen despite its presence in tick salivary glands. As both C. burnetii and numerous “Coxiella-like bacteria” have been reported from several species of ticks, we determined the evolutionary relationship between the two bacteria. Phylogeny estimation revealed that CLEAA is a close relative of C. burnetii, but was not derived from it. Our results are important for strategies geared toward controlling A. americanum and the pathogens it vectors, and also contribute novel information regarding the metabolic interdependencies of ticks and their nutrient-provisioning endosymbionts.
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spelling pubmed-49947182016-08-24 A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick Smith, Todd A Driscoll, Timothy Gillespie, Joseph J Raghavan, Rahul Genome Biol Evol Genome Report Amblyomma americanum (Lone star tick) is an important disease vector in the United States. It transmits several human pathogens, including the agents of human monocytic ehrlichiosis, tularemia, and southern tick-associated rash illness. Blood-feeding insects (Class Insecta) depend on bacterial endosymbionts to provide vitamins and cofactors that are scarce in blood. It is unclear how this deficiency is compensated in ticks (Class Arachnida) that feed exclusively on mammalian blood. A bacterium related to Coxiella burnetii, the agent of human Q fever, has been observed previously within cells of A. americanum. Eliminating this bacterium (CLEAA, Coxiella-like endosymbiont of A. americanum) with antibiotics reduced tick fecundity, indicating that it is an essential endosymbiont. In an effort to determine its role within this symbiosis, we sequenced the CLEAA genome. While highly reduced (656,901 bp) compared with C. burnetii (1,995,281 bp), the CLEAA genome encodes most major vitamin and cofactor biosynthesis pathways, implicating CLEAA as a vitamin provisioning endosymbiont. In contrast, CLEAA lacks any recognizable virulence genes, indicating that it is not a pathogen despite its presence in tick salivary glands. As both C. burnetii and numerous “Coxiella-like bacteria” have been reported from several species of ticks, we determined the evolutionary relationship between the two bacteria. Phylogeny estimation revealed that CLEAA is a close relative of C. burnetii, but was not derived from it. Our results are important for strategies geared toward controlling A. americanum and the pathogens it vectors, and also contribute novel information regarding the metabolic interdependencies of ticks and their nutrient-provisioning endosymbionts. Oxford University Press 2015-01-23 /pmc/articles/PMC4994718/ /pubmed/25618142 http://dx.doi.org/10.1093/gbe/evv016 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Genome Report
Smith, Todd A
Driscoll, Timothy
Gillespie, Joseph J
Raghavan, Rahul
A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title_full A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title_fullStr A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title_full_unstemmed A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title_short A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick
title_sort coxiella-like endosymbiont is a potential vitamin source for the lone star tick
topic Genome Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994718/
https://www.ncbi.nlm.nih.gov/pubmed/25618142
http://dx.doi.org/10.1093/gbe/evv016
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