The midgut of Cephalotes ants (Formicidae: Myrmicinae): Ultrastructure of the epithelium and symbiotic bacteria

Bution, Murillo Lino; Caetano, Flávio Henrique

doi:10.1016/j.micron.2010.02.005

Cited by 14 publications

(14 citation statements)

References 9 publications

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“…This finding, combined with previous localization of many of the studied Cephalotes bacteria to the gut environment (Roche & Wheeler 1997; Russell et al. 2009; Bution & Caetano 2010a,b), suggests that the elucidated cephalotine communities are largely gut associated. This is likely true for several bacteria identified from other ants in this study.…”

Section: Discussionsupporting

confidence: 65%

Highly similar microbial communities are shared among related and trophically similar ant species

et al. 2012

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Ants dominate many terrestrial ecosystems, yet we know little about their nutritional physiology and ecology. While traditionally viewed as predators and scavengers, recent isotopic studies revealed that many dominant ant species are functional herbivores. As with other insects with nitrogen-poor diets, it is hypothesized that these ants rely on symbiotic bacteria for nutritional supplementation. In this study, we used cloning and 16S sequencing to further characterize the bacterial flora of several herbivorous ants, while also examining the beta diversity of bacterial communities within and between ant species from different trophic levels. Through estimating phylogenetic overlap between these communities, we tested the hypothesis that ecologically or phylogenetically similar groups of ants harbor similar microbial flora. Our findings reveal: (i) clear differences in bacterial communities harbored by predatory and herbivorous ants; (ii) notable similarities among communities from distantly related herbivorous ants and (iii) similar communities shared by different predatory army ant species. Focusing on one herbivorous ant tribe, the Cephalotini, we detected five major bacterial taxa that likely represent the core microbiota. Metabolic functions of bacterial relatives suggest that these microbes may play roles in fixing, recycling, or upgrading nitrogen. Overall, our findings reveal that similar microbial communities are harbored by ants from similar trophic niches and, to a greater extent, by related ants from the same colonies, species, genera, and tribes. These trends hint at coevolved histories between ants and microbes, suggesting new possibilities for roles of bacteria in the evolution of both herbivores and carnivores from the ant family Formicidae.

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Section: Discussionsupporting

confidence: 65%

Highly similar microbial communities are shared among related and trophically similar ant species

et al. 2012

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“…(57). The ileum-the anterior region of the hindgut-possesses structural adaptations harboring microbial symbionts (58,59), while bacteria are also found in association with microvilli in the midgut (60,61). In Tetraponera (subfamily Pseudomyrmecinae), a pouch in the ileum harbors symbiotic bacteria (62,63).…”

Section: Discussionmentioning

confidence: 99%

Surveying the Microbiome of Ants: Comparing 454 Pyrosequencing with Traditional Methods To Uncover Bacterial Diversity

Kautz

Rubin

Russell

et al. 2013

Appl Environ Microbiol

112

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We are only beginning to understand the depth and breadth of microbial associations across the eukaryotic tree of life. Reliably assessing bacterial diversity is a key challenge, and next-generation sequencing approaches are facilitating this endeavor. In this study, we used 16S rRNA amplicon pyrosequencing to survey microbial diversity in ants. We compared 454 libraries with Sanger-sequenced clone libraries as well as cultivation of live bacteria. Pyrosequencing yielded 95,656 bacterial 16S rRNA reads from 19 samples derived from four colonies of one ant species. The most dominant bacterial orders in the microbiome of the turtle ant Cephalotes varians were Rhizobiales, Burkholderiales, Opitutales, Xanthomonadales, and Campylobacterales, as revealed through both 454 sequencing and cloning. Even after stringent quality filtering, pyrosequencing recovered 445 microbe operational taxonomic units (OTUs) not detected with traditional techniques. In comparing bacterial communities associated with specific tissues, we found that gut tissues had significantly higher diversity than nongut tissues, and many of the OTUs identified from these groups clustered within ant-specific lineages, indicating a deep coevolutionary history of Cephalotes ants and their associated microbes. These lineages likely function as nutritional symbionts. One of four ant colonies investigated was infected with a Spiroplasma sp. (order Entomoplasmatales), a potential ant pathogen. Our work shows that the microbiome associated with Cephalotes varians is dominated by a few dozen bacterial lineages and that 454 sequencing is a cost-efficient tool to screen ant symbiont diversity.

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“…We therefore examined the gut compartments of 20 ants fed 0.2 μm fluorescent beads using a Zeiss 510 Meta Laser scanning confocal microscope on an Axioimager Z1 with a × 40 oil plan fluor NA 1.3 lens (Carl Zeiss Microscopy LLC, Thornwood, NY, USA), under which the 0.2-μm beads appeared clearly. Each gut compartment was first searched for the presence of beads visually using the multi-track line scan for the fluorescein isothiocyanate and Rhodamine filters at × 400, under which beads appeared bright bluish green and autofluorescent structures such as chitin and spherocrystals ( Bution and Caetano, 2010 ) appeared yellow–green, making them easy to distinguish. Each slide was separately examined by MCL or PAPR, who dissected the ants, and PJ, who had no prior expectation of the location of beads or of the gut compartment being viewed.…”

Section: Methodsmentioning

confidence: 99%

A bacterial filter protects and structures the gut microbiome of an insect

et al. 2016

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Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant (Cephalotes rohweri), blocking the entry of bacteria and particles ⩾0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral–rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host–microbe fidelity both during the animal life cycle and over evolutionary time.

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The midgut of Cephalotes ants (Formicidae: Myrmicinae): Ultrastructure of the epithelium and symbiotic bacteria

Cited by 14 publications

References 9 publications

Highly similar microbial communities are shared among related and trophically similar ant species

Highly similar microbial communities are shared among related and trophically similar ant species

Surveying the Microbiome of Ants: Comparing 454 Pyrosequencing with Traditional Methods To Uncover Bacterial Diversity

A bacterial filter protects and structures the gut microbiome of an insect

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