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One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects.

ABSTRACT: Bacterial endosymbiosis has a recurring significance in the evolution of insects. An estimated 10-20% of insect species depend on bacterial associates for their nutrition and reproductive viability. Members of the ant tribe Camponotini, the focus of this study, possess a stable, intracellular bacterial mutualist. The bacterium, Blochmannia, was first discovered in Camponotus and has since been documented in a distinct subgenus of Camponotus, Colobopsis, and in the related genus Polyrhachis. However, the distribution of Blochmannia throughout the Camponotini remains in question. Documenting the true host range of this bacterial mutualist is an important first step toward understanding the various ecological contexts in which it has evolved, and toward identifying its closest bacterial relatives. In this study, we performed a molecular screen, based on PCR amplification of 16S rDNA, to identify bacterial associates of diverse Camponotini species.Phylogenetic analyses of 16S rDNA gave four important insights: (i) Blochmannia occurs in a broad range of Camponotini genera including Calomyrmex, Echinopla, and Opisthopsis, and did not occur in outgroups related to this tribe (e.g., Notostigma). This suggests that the mutualism originated in the ancestor of the tribe Camponotini. (ii) The known bacteriocyte-associated symbionts of ants, in Formica, Plagiolepis, and the Camponotini, arose independently. (iii) Blochmannia is nestled within a diverse clade of endosymbionts of sap-feeding hemipteran insects, such as mealybugs, aphids, and psyllids. In our analyses, a group of secondary symbionts of mealybugs are the closest relatives of Blochmannia. (iv) Blochmannia has cospeciated with its known hosts, although deep divergences at the genus level remain uncertain.The Blochmannia mutualism occurs in Calomyrmex, Echinopla, and Opisthopsis, in addition to Camponotus, and probably originated in the ancestral lineage leading to the Camponotini. This significant expansion of its known host range implies that the mutualism is more ancient and ecologically diverse than previously documented. Blochmannia is most closely related to endosymbionts of sap-feeding hemipterans, which ants tend for their carbohydrate-rich honeydew. Based on phylogenetic results, we propose Camponotini might have originally acquired this bacterial mutualist through a nutritional symbiosis with other insects.

SUBMITTER: Wernegreen JJ

PROVIDER: S-EPMC2810300 | biostudies-literature | 2009 Dec

REPOSITORIES: biostudies-literature

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One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects.

Wernegreen Jennifer J JJ Kauppinen Seth N SN Brady Seán G SG Ward Philip S PS

BMC evolutionary biology 20091216

<h4>Background</h4>Bacterial endosymbiosis has a recurring significance in the evolution of insects. An estimated 10-20% of insect species depend on bacterial associates for their nutrition and reproductive viability. Members of the ant tribe Camponotini, the focus of this study, possess a stable, intracellular bacterial mutualist. The bacterium, Blochmannia, was first discovered in Camponotus and has since been documented in a distinct subgenus of Camponotus, Colobopsis, and in the related genu ...[more]

PMID: 20015388

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Project description:Stable associations between bacterial endosymbionts and insect hosts provide opportunities to explore genome evolution in the context of established mutualisms and assess the roles of selection and genetic drift across host lineages and habitats. Blochmannia, obligate endosymbionts of ants of the tribe Camponotini, have coevolved with their ant hosts for ∼40 MY. To investigate early events in Blochmannia genome evolution across this ant host tribe, we sequenced Blochmannia from two divergent host lineages, Colobopsis obliquus and Polyrhachis turneri, and compared them with four published genomes from Blochmannia of Camponotus sensu stricto. Reconstructed gene content of the last common ancestor (LCA) of these six Blochmannia genomes is reduced (690 protein coding genes), consistent with rapid gene loss soon after establishment of the symbiosis. Differential gene loss among Blochmannia lineages has affected cellular functions and metabolic pathways, including DNA replication and repair, vitamin biosynthesis and membrane proteins. Blochmannia of P. turneri (i.e., B. turneri) encodes an intact DnaA chromosomal replication initiation protein, demonstrating that loss of dnaA was not essential for establishment of the symbiosis. Based on gene content, B. obliquus and B. turneri are unable to provision hosts with riboflavin. Of the six sequenced Blochmannia, B. obliquus is the earliest diverging lineage (i.e., the sister group of other Blochmannia sampled) and encodes the fewest protein-coding genes and the most pseudogenes. We identified 55 genes involved in parallel gene loss, including glutamine synthetase, which may participate in nitrogen recycling. Pathways for biosynthesis of coenzyme A, terpenoids and riboflavin were lost in multiple lineages, suggesting relaxed selection on the pathway after inactivation of one component. Analysis of Illumina read datasets did not detect evidence of plasmids encoding missing functions, nor the presence of coresident symbionts other than Wolbachia. Although gene order is strictly conserved in four Blochmannia of Camponotus sensu stricto, comparisons with deeply divergent lineages revealed inversions in eight genomic regions, indicating ongoing recombination despite ancestral loss of recA. In sum, the addition of two Blochmannia genomes of divergent host lineages enables reconstruction of early events in evolution of this symbiosis and suggests that Blochmannia lineages may experience distinct, host-associated selective pressures. Understanding how evolutionary forces shape genome reduction in this system may help to clarify forces driving gene loss in other bacteria, including intracellular pathogens.

Project description:BackgroundCarpenter 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.ResultsNutritional 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 15N-labelled urea. GC-MS analysis of 15N-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.ConclusionOur 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.

Project 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. 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 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.

Project description:This study investigated the effects of ant attendance on the parasitoid community and parasitism of lac insect Kerria yunnanensis aggregations in Yunnan province, China. We manipulated ant attendance to establish three treatments: (1) ant exclusion; (2) low ant attendance by several ant species; and (3) high ant attendance by Crematogaster macaoensis. Five parasitoid species were collected, with two species contributing 82.7 and 13.2% of total abundance respectively. Total parasitoid abundance was lowest in the February sample when K. yunnanensis was in its younger life stage, being significantly lower in the ant exclusion treatment. In April, all three treatments had significantly different parasitoid abundances, being highest in the ant exclusion treatment and the lowest in the high ant attendance treatment. When ants were present, there were strong negative relationships between total parasitoid abundance and ant abundance, with the relationships being dependent upon the ant species composition and abundance. The patterns of total parasitoid abundance were driven by the two most abundant parasitoid species. Parasitoid species richness did not differ among treatments or between sample times, however, multivariate analysis confirmed that overall parasitoid community structure differed significantly among treatments and between sample times, with the high ant attendance treatment differing most from the other two treatments. Interestingly the absence of ants did not result in increased parasitism from four of the five parasitoids. Ants in lac insect farming systems have a clear role for agricultural pest management. A full understanding of the asymmetric abilities of ants to influence parasitoid communities, and affect parasitism of hosts will require further experimental manipulation to assess the relative roles of 1) the abundance of each individual ant species on parasitoid access to hosts, 2) competition among parasitoids, and 3) the interaction between the first two factors.

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One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects.

Publications

One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects.

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