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

Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg-Bauer E, Bouffard P, Caldera EJ, Cash E, Cavanaugh A, Denas O, Elhaik E, Favé MJ, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Harkins TT, Helmkampf M, Hu H, Johnson BR, Kim J, Marsh SE, Moeller JA, Muñoz-Torres MC, Murphy MC, Naughton MC, Nigam S, Overson R, Rajakumar R, Reese JT, Scott JJ, Smith CR, Tao S, Tsutsui ND, Viljakainen L, Wissler L, Yandell MD, Zimmer F, Taylor J, Slater SC, Clifton SW, Warren WC, Elsik CG, Smith CD, Weinstock GM, Gerardo NM, Currie CR - PLoS Genet. (2011)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America. gsuen@wisc.edu

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.

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Distribution of hexamerin genes in the genomes of Atta cephalotes, Camponotus floridanus, Harpegnathos saltator, Apis mellifera, and Nasonia vitripennis.Four hexamerins with varying copy number are found within these genomes except for A. cephalotes which is missing hex 70c. Many of these genes are found to be syntenic along chromosomes/scaffolds, as shown (not drawn to scale).
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pgen-1002007-g004: Distribution of hexamerin genes in the genomes of Atta cephalotes, Camponotus floridanus, Harpegnathos saltator, Apis mellifera, and Nasonia vitripennis.Four hexamerins with varying copy number are found within these genomes except for A. cephalotes which is missing hex 70c. Many of these genes are found to be syntenic along chromosomes/scaffolds, as shown (not drawn to scale).

Mentions: In addition to arginine biosynthesis, A. cephalotes may have also lost the need to rely on hexamerins as a source of amino acids during development. In many insects, hexamerin proteins are synthesized by developing larvae and used as amino acid sources during development into the adult stage [74]. Four hexamerins are commonly found across insects, including hex 70a, hex 70b, hex 70c, and hex 110. Comparison among the hymenopteran genomes reveals the presence of all hexamerins in varying copy number across all genomes except for A. cephalotes, which is missing hex 70c (Figure 4) (Text S16). In A. mellifera, hexamerins are expressed at different times, with hex 70a and hex 110 expressed during the larval, pupal and adult stage of workers, and hex 70b and hex 70c only expressed during the larval stage [74]. The specific expression of hex 70b and hex 70c in larvae may reflect the increased need for these nutrients during early development. Given that A. cephalotes larvae feed primarily on gongylidia, it is possible that amino acids supplemented by the fungus over the millions of years of this mutualism has relaxed selection for maintaining larval-stage hexamerins, and thus hex 70c may have been lost. 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.


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

Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg-Bauer E, Bouffard P, Caldera EJ, Cash E, Cavanaugh A, Denas O, Elhaik E, Favé MJ, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Harkins TT, Helmkampf M, Hu H, Johnson BR, Kim J, Marsh SE, Moeller JA, Muñoz-Torres MC, Murphy MC, Naughton MC, Nigam S, Overson R, Rajakumar R, Reese JT, Scott JJ, Smith CR, Tao S, Tsutsui ND, Viljakainen L, Wissler L, Yandell MD, Zimmer F, Taylor J, Slater SC, Clifton SW, Warren WC, Elsik CG, Smith CD, Weinstock GM, Gerardo NM, Currie CR - PLoS Genet. (2011)

Distribution of hexamerin genes in the genomes of Atta cephalotes, Camponotus floridanus, Harpegnathos saltator, Apis mellifera, and Nasonia vitripennis.Four hexamerins with varying copy number are found within these genomes except for A. cephalotes which is missing hex 70c. Many of these genes are found to be syntenic along chromosomes/scaffolds, as shown (not drawn to scale).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3037820&req=5

pgen-1002007-g004: Distribution of hexamerin genes in the genomes of Atta cephalotes, Camponotus floridanus, Harpegnathos saltator, Apis mellifera, and Nasonia vitripennis.Four hexamerins with varying copy number are found within these genomes except for A. cephalotes which is missing hex 70c. Many of these genes are found to be syntenic along chromosomes/scaffolds, as shown (not drawn to scale).
Mentions: In addition to arginine biosynthesis, A. cephalotes may have also lost the need to rely on hexamerins as a source of amino acids during development. In many insects, hexamerin proteins are synthesized by developing larvae and used as amino acid sources during development into the adult stage [74]. Four hexamerins are commonly found across insects, including hex 70a, hex 70b, hex 70c, and hex 110. Comparison among the hymenopteran genomes reveals the presence of all hexamerins in varying copy number across all genomes except for A. cephalotes, which is missing hex 70c (Figure 4) (Text S16). In A. mellifera, hexamerins are expressed at different times, with hex 70a and hex 110 expressed during the larval, pupal and adult stage of workers, and hex 70b and hex 70c only expressed during the larval stage [74]. The specific expression of hex 70b and hex 70c in larvae may reflect the increased need for these nutrients during early development. Given that A. cephalotes larvae feed primarily on gongylidia, it is possible that amino acids supplemented by the fungus over the millions of years of this mutualism has relaxed selection for maintaining larval-stage hexamerins, and thus hex 70c may have been lost. 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.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America. gsuen@wisc.edu

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.

Show MeSH
Related in: MedlinePlus