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Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia

BACKGROUND: Carpenter ants (genus Camponotus) are considered to be omnivores. Nonetheless, the genome sequence of Blochmannia floridanus, the obligate intracellular endosymbiont of Camponotus floridanus, suggests a function in nutritional upgrading of host resources by the bacterium. Thus, the stron...

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Autores principales: Feldhaar, Heike, Straka, Josef, Krischke, Markus, Berthold, Kristina, Stoll, Sascha, Mueller, Martin J, Gross, Roy
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2007
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2206011/
https://www.ncbi.nlm.nih.gov/pubmed/17971224
http://dx.doi.org/10.1186/1741-7007-5-48
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author Feldhaar, Heike
Straka, Josef
Krischke, Markus
Berthold, Kristina
Stoll, Sascha
Mueller, Martin J
Gross, Roy
author_facet Feldhaar, Heike
Straka, Josef
Krischke, Markus
Berthold, Kristina
Stoll, Sascha
Mueller, Martin J
Gross, Roy
author_sort Feldhaar, Heike
collection PubMed
description BACKGROUND: Carpenter ants (genus Camponotus) are considered to be omnivores. Nonetheless, the genome sequence of Blochmannia floridanus, the obligate intracellular endosymbiont of Camponotus floridanus, suggests a function in nutritional upgrading of host resources by the bacterium. Thus, the strongly reduced genome of the endosymbiont retains genes for all subunits of a functional urease, as well as those for biosynthetic pathways for all but one (arginine) of the amino acids essential to the host. RESULTS: Nutritional upgrading by Blochmannia was tested in 90-day feeding experiments with brood-raising in worker-groups on chemically defined diets with and without essential amino acids and treated or not with antibiotics. Control groups were fed with cockroaches, honey water and Bhatkar agar. Worker-groups were provided with brood collected from the queenright mother-colonies (45 eggs and 45 first instar larvae each). Brood production did not differ significantly between groups of symbiotic workers on diets with and without essential amino acids. However, aposymbiotic worker groups raised significantly less brood on a diet lacking essential amino acids. Reduced brood production by aposymbiotic workers was compensated when those groups were provided with essential amino acids in their diet. Decrease of endosymbionts due to treatment with antibiotic was monitored by qRT-PCR and FISH after the 90-day experimental period. Urease function was confirmed by feeding experiments using (15)N-labelled urea. GC-MS analysis of (15)N-enrichment of free amino acids in workers revealed significant labelling of the non-essential amino acids alanine, glycine, aspartic acid, and glutamic acid, as well as of the essential amino acids methionine and phenylalanine. CONCLUSION: Our results show that endosymbiotic Blochmannia nutritionally upgrade the diet of C. floridanus hosts to provide essential amino acids, and that it may also play a role in nitrogen recycling via its functional urease. Blochmannia may confer a significant fitness advantage via nutritional upgrading by enhancing competitive ability of Camponotus with other ant species lacking such an endosymbiont. Domestication of the endosymbiont may have facilitated the evolutionary success of the genus Camponotus.
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spelling pubmed-22060112008-01-18 Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia Feldhaar, Heike Straka, Josef Krischke, Markus Berthold, Kristina Stoll, Sascha Mueller, Martin J Gross, Roy BMC Biol Research Article BACKGROUND: Carpenter ants (genus Camponotus) are considered to be omnivores. Nonetheless, the genome sequence of Blochmannia floridanus, the obligate intracellular endosymbiont of Camponotus floridanus, suggests a function in nutritional upgrading of host resources by the bacterium. Thus, the strongly reduced genome of the endosymbiont retains genes for all subunits of a functional urease, as well as those for biosynthetic pathways for all but one (arginine) of the amino acids essential to the host. RESULTS: Nutritional upgrading by Blochmannia was tested in 90-day feeding experiments with brood-raising in worker-groups on chemically defined diets with and without essential amino acids and treated or not with antibiotics. Control groups were fed with cockroaches, honey water and Bhatkar agar. Worker-groups were provided with brood collected from the queenright mother-colonies (45 eggs and 45 first instar larvae each). Brood production did not differ significantly between groups of symbiotic workers on diets with and without essential amino acids. However, aposymbiotic worker groups raised significantly less brood on a diet lacking essential amino acids. Reduced brood production by aposymbiotic workers was compensated when those groups were provided with essential amino acids in their diet. Decrease of endosymbionts due to treatment with antibiotic was monitored by qRT-PCR and FISH after the 90-day experimental period. Urease function was confirmed by feeding experiments using (15)N-labelled urea. GC-MS analysis of (15)N-enrichment of free amino acids in workers revealed significant labelling of the non-essential amino acids alanine, glycine, aspartic acid, and glutamic acid, as well as of the essential amino acids methionine and phenylalanine. CONCLUSION: Our results show that endosymbiotic Blochmannia nutritionally upgrade the diet of C. floridanus hosts to provide essential amino acids, and that it may also play a role in nitrogen recycling via its functional urease. Blochmannia may confer a significant fitness advantage via nutritional upgrading by enhancing competitive ability of Camponotus with other ant species lacking such an endosymbiont. Domestication of the endosymbiont may have facilitated the evolutionary success of the genus Camponotus. BioMed Central 2007-10-30 /pmc/articles/PMC2206011/ /pubmed/17971224 http://dx.doi.org/10.1186/1741-7007-5-48 Text en Copyright © 2007 Feldhaar 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
Feldhaar, Heike
Straka, Josef
Krischke, Markus
Berthold, Kristina
Stoll, Sascha
Mueller, Martin J
Gross, Roy
Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title_full Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title_fullStr Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title_full_unstemmed Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title_short Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia
title_sort nutritional upgrading for omnivorous carpenter ants by the endosymbiont blochmannia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2206011/
https://www.ncbi.nlm.nih.gov/pubmed/17971224
http://dx.doi.org/10.1186/1741-7007-5-48
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