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.

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

“…1e) Table 7). Ornithine carbamoyl-transferase (EC 2.1.3.3) was not found among any of the five Hymenopteran insects (A. cephalotes, Camponotus floridanus, Harpegnathus saltator, Apis mellifera, Nasonia vitripennis) that were previously analysed 34 , but was also identified in the L. gongylophorus transcriptome. (b) Two genes coding for enzymes mediating aromatic amino acids biosynthesis, chorismate mutase (EC 5.4.99.5) and aminotransferase (EC 2.6.1.1), had alleles that were significantly upregulated in the gongylidia (Supplementary Table 8), indicating that the essential amino acids phenylalanine and tyrosine are produced in high amounts in the gongylidia.…”

“…The recently sequenced genomes of A. echinatior and A. cephalotes showed that these two leaf-cutting ants lack two essential genes for arginine biosynthesis that three other genome-sequenced ant species with normal hunter-gatherer life styles have retained 33,34 . Both papers hypothesized that the ensuing inability of these ants to synthesize arginine would probably be compensated by metabolic activities of the fungus-garden symbiont.…”

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…We annotated CSP genes in seven published ant genomes (C. floridanus, Harpegnathos saltator, S. invicta, L. humile, Pogonomyrmex barbatus, Acromyrmex echinatior and Atta cephalotes) (Bonasio et al, 2010;Nygaard et al, 2011;Suen et al, 2011;Wurm et al, 2011) (Figure 1). The abbreviations used here are, respectively, Cflo, Hsal, Sinv, Lhum, Pbar, Aech and Acep.…”

Advances in genomics for flatfish aquaculture

“…Although limited information about sequencing strategies and assemblies is still available, length reads and strategies to orientate adequately the scaffolds and contigs are critical. For the Senegalese sole, as in other de novo eukaryotic genomes published until now, a two-step strategy is being followed: scaffolding using matepair (Illumina Ò ) and long paired-end libraries (454) with insert sizes comprised between 2 kb and 20 kb, followed by massive whole-genome shotgun sequencing (454 and Illumina paired-ends) to be assembled into smaller contigs (Huang et al 2009;Dalloul et al 2010;Li et al 2010;Suen et al 2011;Woycicki et al 2011). However, de novo assembly of large and complex eukaryotic genomes is still challenging due to repetitive DNA and, in fish, by additional whole-genome duplication (WGD) events that occurred in the teleost lineage (3R and 4R in salmonids).…”