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The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

ABSTRACT: Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host-microbe symbioses.

SUBMITTER: Suen G

PROVIDER: S-EPMC3037820 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

Suen Garret G Teiling Clotilde C Li Lewyn L Holt Carson C Abouheif Ehab E Bornberg-Bauer Erich E Bouffard Pascal P Caldera Eric J EJ Cash Elizabeth E Cavanaugh Amy A Denas Olgert O Elhaik Eran E Favé Marie-Julie MJ Gadau Jürgen J Gibson Joshua D JD Graur Dan D Grubbs Kirk J KJ Hagen Darren E DE Harkins Timothy T TT Helmkampf Martin M Hu Hao H Johnson Brian R BR Kim Jay J Marsh Sarah E SE Moeller Joseph A JA Muñoz-Torres Mónica C MC Murphy Marguerite C MC Naughton Meredith C MC Nigam Surabhi S Overson Rick R Rajakumar Rajendhran R Reese Justin T JT Scott Jarrod J JJ Smith Chris R CR Tao Shu S Tsutsui Neil D ND Viljakainen Lumi L Wissler Lothar L Yandell Mark D MD Zimmer Fabian F Taylor James J Slater Steven C SC Clifton Sandra W SW Warren Wesley C WC Elsik Christine G CG Smith Christopher D CD Weinstock George M GM Gerardo Nicole M NM Currie Cameron R CR

PLoS genetics 20110210 2

Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldier ...[more]

PMID: 21347285

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Project description:BackgroundLeaf-cutter ants use fresh plant material to grow a mutualistic fungus that serves as the ants' primary food source. Within fungus gardens, various plant compounds are metabolized and transformed into nutrients suitable for ant consumption. This symbiotic association produces a large amount of refuse consisting primarily of partly degraded plant material. A leaf-cutter ant colony is thus divided into two spatially and chemically distinct environments that together represent a plant biomass degradation gradient. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies.Methodology/principal findingsUsing microbial membrane lipid analysis and a variety of community metrics, we assessed and compared the microbiota of fungus gardens and refuse dumps from both laboratory-maintained and field-collected colonies. We found that gardens contained a diverse and consistent community of microbes, dominated by Gram-negative bacteria, particularly gamma-Proteobacteria and Bacteroidetes. These findings were consistent across lab and field gardens, as well as host ant taxa. In contrast, dumps were enriched for Gram-positive and anaerobic bacteria. Broad-scale clustering analyses revealed that community relatedness between samples reflected system component (gardens/dumps) rather than colony source (lab/field). At finer scales samples clustered according to colony source.Conclusions/significanceHere we report the first comparative analysis of the microbiota from leaf-cutter ant colonies. Our work reveals the presence of two distinct communities: one in the fungus garden and the other in the refuse dump. Though we find some effect of colony source on community structure, our data indicate the presence of consistently associated microbes within gardens and dumps. Substrate composition and system component appear to be the most important factor in structuring the microbial communities. These results thus suggest that resident communities are shaped by the plant degradation gradient created by ant behavior, specifically their fungiculture and waste management.

Project description:Background:Ecosystem engineers are species that transform habitats in ways that influence other species.While the impacts of many engineers have been well described, our understanding of how their impact varies along environmental gradients remains limited. Although disentangling the effects of gradients and engineers on biodiversity is complicated-the gradients themselves can be altered by engineers-doing so is necessary to advance conceptual and mathematical models of ecosystem engineering. We used leaf-cutter ants (Atta spp.) to investigate the relative influence of gradients and environmental engineers on the abundance and species richness of woody plants. Methods:We conducted our research in South America's Cerrado. With a survey of plant recruits along a canopy cover gradient, and data on environmental conditions that influence plant recruitment, we fit statistical models that addressed the following questions: (1) Does A. laevigata modify the gradient in canopy cover found in our Cerrado site? (2) Do environmental conditions that influence woody plant establishment in the Cerrado vary with canopy cover or proximity to A. laevigata nests? (3) Do A. laevigata and canopy cover act independently or in concert to influence recruit abundance and species richness? Results:We found that environmental conditions previously shown to influence plant establishment in the Cerrado varied in concert with canopy cover, but that ants are not modifying the cover gradient or cover over nests. However, ants are modifying other local environmental conditions, and the magnitude and spatial extent of these changes are consistent across the gradient. In contrast to prior studies, we found that ant-related factors (e.g., proximity to nests, ant changes in surface conditions), rather than canopy cover, had the strongest effect on the abundance of plant recruits. However, the diversity of plants was influenced by both the engineer and the canopy cover gradient. Discussion:Atta laevigata in the Cerrado modify local conditions in ways that have strong but spatially restricted consequences for plant communities. We hypothesize that ants indirectly reduce seedling establishment by clearing litter and reducing soil moisture, which leads to seed and seedling desiccation. Altering soil nutrients could also reduce juvenile growth and survivorship; if so these indirect negative effects of engineering could exacerbate their direct effects of harvesting plants. The effects of Atta appear restricted to nest mounds, but they could be long-lasting because mounds persist long after a colony has died or migrated. Our results support the hypothesis that leaf-cutter ants play a dominant role in Cerrado plant demography. We suggest the ecological and economic footprint of these engineers may increase dramatically in coming decades due to the transformation of the Cerrado by human activities.

Dataset Information

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

Publications

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

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