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.
Highlights
Ants are one of the most successful insects on earth, comprising up to 20% of all terrestrial animal biomass and at least 25% of the entire animal biomass in the New World Tropics [1]
When genes are mapped to compositional domains in the A. cephalotes genome, we find that they are uniformly distributed across the entire genome, in contrast to N. vitripennis and A. mellifera, which have genes occurring in more GCpoor regions of their genomes
We have provided some evidence that A. cephalotes has gene reductions related to nutrient acquisition, and these losses may be compensated by the provision of these nutrients from the fungus
Summary
Ants are one of the most successful insects on earth, comprising up to 20% of all terrestrial animal biomass and at least 25% of the entire animal biomass in the New World Tropics [1]. To gain a better understanding of the biology of leaf-cutter ants, we sequenced the genome of Atta cephalotes using 454 pyrosequencing technology [25] and generated a high-quality de novo assembly and annotation Analysis of this genome sequence reveals a loss of genes associated with nutrient acquisition and amino acid biosynthesis. Honey dew is a major component of the diet of C. floridanus and contains primarily sugars [1], while the honey/pollen diet of A. mellifera is composed primarily of carbohydrates, lipids, carbohydrates, vitamins, and some proteins [66] Because this under-representation of trypsin is consistent across social insects when compared to other sequenced insects (Table S5, Text S14), this reduction may reflect the specific dietary features of these insects, or could indicate a loss of these genes across eusocial insects. Future expression analyses of these genes at different life stages, in different castes, and under different nutritional conditions will likely confirm and elucidate their role
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