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Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah

BACKGROUND: Microorganisms are a large and diverse form of life. Many of them live in association with large multicellular organisms, developing symbiotic relations with the host and some have even evolved to form obligate endosymbiosis [1]. All Carpenter ants (genus Camponotus) studied hitherto har...

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Autores principales: de Souza, Danival J, Bézier, Annie, Depoix, Delphine, Drezen, Jean-Michel, Lenoir, Alain
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2660346/
https://www.ncbi.nlm.nih.gov/pubmed/19200360
http://dx.doi.org/10.1186/1471-2180-9-29
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author de Souza, Danival J
Bézier, Annie
Depoix, Delphine
Drezen, Jean-Michel
Lenoir, Alain
author_facet de Souza, Danival J
Bézier, Annie
Depoix, Delphine
Drezen, Jean-Michel
Lenoir, Alain
author_sort de Souza, Danival J
collection PubMed
description BACKGROUND: Microorganisms are a large and diverse form of life. Many of them live in association with large multicellular organisms, developing symbiotic relations with the host and some have even evolved to form obligate endosymbiosis [1]. All Carpenter ants (genus Camponotus) studied hitherto harbour primary endosymbiotic bacteria of the Blochmannia genus. The role of these bacteria in ant nutrition has been demonstrated [2] but the omnivorous diet of these ants lead us to hypothesize that the bacteria might provide additional advantages to their host. In this study, we establish links between Blochmannia, growth of starting new colonies and the host immune response. RESULTS: We manipulated the number of bacterial endosymbionts in incipient laboratory-reared colonies of Camponotus fellah by administrating doses of an antibiotic (Rifampin) mixed in honey-solution. Efficiency of the treatment was estimated by quantitative polymerase chain reaction and Fluorescent in situ hybridization (FISH), using Blochmannia specific primers (qPCR) and two fluorescent probes (one for all Eubacterial and other specific for Blochmannia). Very few or no bacteria could be detected in treated ants. Incipient Rifampin treated colonies had significantly lower numbers of brood and adult workers than control colonies. The immune response of ants from control and treated colonies was estimated by inserting nylon filaments in the gaster and removing it after 24 h. In the control colonies, the encapsulation response was positively correlated to the bacterial amount, while no correlation was observed in treated colonies. Indeed, antibiotic treatment increased the encapsulation response of the workers, probably due to stress conditions. CONCLUSION: The increased growth rate observed in non-treated colonies confirms the importance of Blochmannia in this phase of colony development. This would provide an important selective advantage during colony founding, where the colonies are faced with severe inter and intraspecific competition. Furthermore, the bacteria improve the workers encapsulation response. Thus, these ants are likely to be less susceptible to various pathogen attacks, such as the Phoridae fly parasitoids, normally found in the vicinity of Camponotus nests. These advantages might explain the remarkable ecological success of this ant genus, comprising more than 1000 species.
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spelling pubmed-26603462009-03-25 Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah de Souza, Danival J Bézier, Annie Depoix, Delphine Drezen, Jean-Michel Lenoir, Alain BMC Microbiol Research article BACKGROUND: Microorganisms are a large and diverse form of life. Many of them live in association with large multicellular organisms, developing symbiotic relations with the host and some have even evolved to form obligate endosymbiosis [1]. All Carpenter ants (genus Camponotus) studied hitherto harbour primary endosymbiotic bacteria of the Blochmannia genus. The role of these bacteria in ant nutrition has been demonstrated [2] but the omnivorous diet of these ants lead us to hypothesize that the bacteria might provide additional advantages to their host. In this study, we establish links between Blochmannia, growth of starting new colonies and the host immune response. RESULTS: We manipulated the number of bacterial endosymbionts in incipient laboratory-reared colonies of Camponotus fellah by administrating doses of an antibiotic (Rifampin) mixed in honey-solution. Efficiency of the treatment was estimated by quantitative polymerase chain reaction and Fluorescent in situ hybridization (FISH), using Blochmannia specific primers (qPCR) and two fluorescent probes (one for all Eubacterial and other specific for Blochmannia). Very few or no bacteria could be detected in treated ants. Incipient Rifampin treated colonies had significantly lower numbers of brood and adult workers than control colonies. The immune response of ants from control and treated colonies was estimated by inserting nylon filaments in the gaster and removing it after 24 h. In the control colonies, the encapsulation response was positively correlated to the bacterial amount, while no correlation was observed in treated colonies. Indeed, antibiotic treatment increased the encapsulation response of the workers, probably due to stress conditions. CONCLUSION: The increased growth rate observed in non-treated colonies confirms the importance of Blochmannia in this phase of colony development. This would provide an important selective advantage during colony founding, where the colonies are faced with severe inter and intraspecific competition. Furthermore, the bacteria improve the workers encapsulation response. Thus, these ants are likely to be less susceptible to various pathogen attacks, such as the Phoridae fly parasitoids, normally found in the vicinity of Camponotus nests. These advantages might explain the remarkable ecological success of this ant genus, comprising more than 1000 species. BioMed Central 2009-02-06 /pmc/articles/PMC2660346/ /pubmed/19200360 http://dx.doi.org/10.1186/1471-2180-9-29 Text en Copyright ©2009 de Souza et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research article
de Souza, Danival J
Bézier, Annie
Depoix, Delphine
Drezen, Jean-Michel
Lenoir, Alain
Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title_full Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title_fullStr Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title_full_unstemmed Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title_short Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah
title_sort blochmannia endosymbionts improve colony growth and immune defence in the ant camponotus fellah
topic Research article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2660346/
https://www.ncbi.nlm.nih.gov/pubmed/19200360
http://dx.doi.org/10.1186/1471-2180-9-29
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