Cloning and sequencing of wsp encoding gene fragments reveals a diversity of co-infecting Wolbachia strains in Acromyrmex leafcutter ants

Borm, Steven Van; Wenseleers, Tom; Billen, Johan; Boomsma, Jacobus J.

doi:10.1016/s1055-7903(02)00298-1

Cited by 51 publications

(71 citation statements)

References 45 publications

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“…Wolbachia has been found in several sexually reproducing ant species ( Wenseleers et al 1998) including fungus-growing ants (Van Borm et al 2003), but is absent in seven partially asexual ant species (Wenseleers & Billen 2000;Fournier et al 2005;Pearcy et al 2005). We document here that endosymbiotic microbes also appear to be absent in the asexual M. smithii.…”

Section: Discussionmentioning

confidence: 57%

No sex in fungus-farming ants or their crops

et al. 2009

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Asexual reproduction imposes evolutionary handicaps on asexual species, rendering them prone to extinction, because asexual reproduction generates novel genotypes and purges deleterious mutations at lower rates than sexual reproduction. Here, we report the first case of complete asexuality in ants, the fungusgrowing ant Mycocepurus smithii, where queens reproduce asexually but workers are sterile, which is doubly enigmatic because the clonal colonies of M. smithii also depend on clonal fungi for food. Degenerate female mating anatomy, extensive field and laboratory surveys, and DNA fingerprinting implicate complete asexuality in this widespread ant species. Maternally inherited bacteria (e.g. Wolbachia, Cardinium) and the fungal cultivars can be ruled out as agents inducing asexuality. M. smithii societies of clonal females provide a unique system to test theories of parent-offspring conflict and reproductive policing in social insects. Asexuality of both ant farmer and fungal crop challenges traditional views proposing that sexual farmer ants outpace coevolving sexual crop pathogens, and thus compensate for vulnerabilities of their asexual crops. Either the double asexuality of both farmer and crop may permit the host to fully exploit advantages of asexuality for unknown reasons or frequent switching between crops (symbiont reassociation) generates novel ant-fungus combinations, which may compensate for any evolutionary handicaps of asexuality in M. smithii.

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Section: Discussionmentioning

confidence: 57%

No sex in fungus-farming ants or their crops

et al. 2009

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“…Horizontal transmission could explain why closely related Wolbachia occur in the distantly related ant genera Acromyrmex, Solenopsis, and Linepithema. The vector of horizontal transmission could have been parasites or parasitoids specialised on ants (van Borm et al, 2003). Finally, it should be noted that sequence similarity might also stem from homologous recombination between Wolbachia lineages.…”

Section: Discussionmentioning

confidence: 99%

Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile

2004

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Wolbachia are maternally inherited bacteria, which are very common in arthropods and nematodes. Wolbachia infection may affect host reproduction through feminisation, parthenogenesis, male-killing, cytoplasmic incompatibility and increased fecundity. Previous studies showing discrepancies between the phylogenies of Wolbachia and its arthropod hosts indicate that infection is frequently lost, but the causes of symbiont extinction have so far remained elusive. Here, we report data showing that colonisation of new habitats is a possible mechanism leading to the loss of infection. The presence and prevalence of Wolbachia were studied in three native and eight introduced populations of the Argentine ant Linepithema humile. The screening shows that the symbiont is common in the three native L. humile populations analysed. In contrast, Wolbachia was detected in only one of the introduced populations. The loss of infection associated with colonisation of new habitats may result from drift (founder effect) or altered selection pressures in the new habitat. Furthermore, a molecular phylogeny based on sequences of the Wolbachia wsp gene indicates that L. humile has been infected by a single strain. Horizontal transmission of the symbiont may be important in ants as suggested by the sequence similarity of strains in the three genera Linepithema, Acromyrmex, and Solenopsis native from South and Central America.

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“…None of the other OTUs was restricted to or specific for any of the three Acromyrmex ant species (see Table S4A in the supplemental material). We further characterized the RhiAcro1, EntAcro1, and EntAcro2 OTUs using Sanger sequencing and obtained 982-bp, 1,282-bp, and 1,340-bp sequences, respectively, while the WolAcro1 OTU has been characterized previously (48,49). Maximum-likelihood phylogenetic trees showed that RhiAcro1 is closely related to Rhizobiales strains identified in Trachymyrmex urichii of the attine lineage (see Fig.…”

Section: S-454 and 16s-miseq Sequencingmentioning

confidence: 99%

Acromyrmex Leaf-Cutting Ants Have Simple Gut Microbiota with Nitrogen-Fixing Potential

Sapountzis

Zhukova

Hansen

et al. 2015

Appl Environ Microbiol

142

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Ants and termites have independently evolved obligate fungus-farming mutualisms, but their gardening procedures are fundamentally different, as the termites predigest their plant substrate whereas the ants deposit it directly on the fungus garden. Fungus-growing termites retained diverse gut microbiota, but bacterial gut communities in fungus-growing leaf-cutting ants have not been investigated, so it is unknown whether and how they are specialized on an exclusively fungal diet. Here we characterized the gut bacterial community of Panamanian Acromyrmex species, which are dominated by only four bacterial taxa: Wolbachia, Rhizobiales, and two Entomoplasmatales taxa. We show that the Entomoplasmatales can be both intracellular and extracellular across different gut tissues, Wolbachia is mainly but not exclusively intracellular, and the Rhizobiales species is strictly extracellular and confined to the gut lumen, where it forms biofilms along the hindgut cuticle supported by an adhesive matrix of polysaccharides. Tetracycline diets eliminated the Entomoplasmatales symbionts but hardly affected Wolbachia and only moderately reduced the Rhizobiales, suggesting that the latter are protected by the biofilm matrix. We show that the Rhizobiales symbiont produces bacterial NifH proteins that have been associated with the fixation of nitrogen, suggesting that these compartmentalized hindgut symbionts alleviate nutritional constraints emanating from an exclusive fungus garden diet reared on a substrate of leaves. Communities of gut bacteria play key roles in nutrient acquisition, vitamin supplementation, and disease resistance. Their diversity often covaries with host diet, both across lineages with different ecological niches and between conspecific populations in different habitats or geographic regions (1-3). Elucidating the significance of single bacterial taxa in omnivores such as humans is dauntingly complex (3, 4), but insects with specialized diets have regularly offered gut microbiota study systems that are dominated by a limited number of species (5-7). Several insect-microbial symbioses are evolutionarily ancient so that extensive functional complementarity between hosts and symbionts could evolve, as in aphids that rely on Buchnera for the production of essential amino acids (8, 9). Other mutualisms have more recent origins, such as bedbugs that rely on Wolbachia for vitamin B production (10, 11) or wood-eating beetles that carry nitrogen-fixing gut bacteria in order to subsist on protein-poor diets (12).The eusocial insects offer abundant niche space for bacterial symbionts (5, 13-16) because many have peculiar diets and practice liquid food transfer (trophallaxis), which facilitates symbiont transmission within colonies. Higher termites replaced their ancestral protist gut communities by bacterial microbiota (17), while other early studies identified Blochmannia gut symbionts in carpenter ants (18, 19) and a community of gut-pouch symbionts in Tetraponera ants (20, 21). More recently, comparative studies have st...

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Cloning and sequencing of wsp encoding gene fragments reveals a diversity of co-infecting Wolbachia strains in Acromyrmex leafcutter ants

Cited by 51 publications

References 45 publications

No sex in fungus-farming ants or their crops

No sex in fungus-farming ants or their crops

Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile

Acromyrmex Leaf-Cutting Ants Have Simple Gut Microbiota with Nitrogen-Fixing Potential

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