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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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Predicted arginine biosynthesis pathway map in Atta cephalotes, Camponotus floridanus, Harpegnathus saltator, Apis mellifera, and Nasonia vitripennis.This pathway in A. cephalotes was found to be missing the two enzymes agininosuccinate synthase (EC 6.3.4.5) and argininosuccinate lyase (EC 4.3.2.1), which catalyzes the conversion of aspartate and citrulline into arginine. Other enzymes in this pathway include ornithine cabamoyltransferase (EC 2.1.3.3), arginase (EC 3.5.3.1) and nitric oxide synthase (EC 1.14.13.39). Dotted arrows indicate genes encoding proteins which were not found.
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pgen-1002007-g003: Predicted arginine biosynthesis pathway map in Atta cephalotes, Camponotus floridanus, Harpegnathus saltator, Apis mellifera, and Nasonia vitripennis.This pathway in A. cephalotes was found to be missing the two enzymes agininosuccinate synthase (EC 6.3.4.5) and argininosuccinate lyase (EC 4.3.2.1), which catalyzes the conversion of aspartate and citrulline into arginine. Other enzymes in this pathway include ornithine cabamoyltransferase (EC 2.1.3.3), arginase (EC 3.5.3.1) and nitric oxide synthase (EC 1.14.13.39). Dotted arrows indicate genes encoding proteins which were not found.

Mentions: Given the tight obligate association that A. cephalotes has with its fungal mutualist, one might predict that it acquires amino acids from its fungus in a manner similar to that of the pea aphid Acyrthosiphon pisum, which obtains amino acids from its bacterial symbionts [28]. To test this, we performed a metabolic reconstruction analysis using the Kyoto Encyclopedia of Genes and Genomes (KEGG) [69]. A. cephalotes contains a nearly identical set of amino acid biosynthesis genes as A. mellifera, C. floridanus, H. saltator, and N. vitripennis, all of which are incapable of synthesizing histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine de novo. The only exception is arginine, and only A. cephalotes was found to lack the genes necessary for its biosynthesis (Figure 3). Arginine, which is produced through the conversion of citrulline and aspartate [70], [71], is predicted to be synthesized at levels too low to support growth in insects [72].


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)

Predicted arginine biosynthesis pathway map in Atta cephalotes, Camponotus floridanus, Harpegnathus saltator, Apis mellifera, and Nasonia vitripennis.This pathway in A. cephalotes was found to be missing the two enzymes agininosuccinate synthase (EC 6.3.4.5) and argininosuccinate lyase (EC 4.3.2.1), which catalyzes the conversion of aspartate and citrulline into arginine. Other enzymes in this pathway include ornithine cabamoyltransferase (EC 2.1.3.3), arginase (EC 3.5.3.1) and nitric oxide synthase (EC 1.14.13.39). Dotted arrows indicate genes encoding proteins which were not found.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1002007-g003: Predicted arginine biosynthesis pathway map in Atta cephalotes, Camponotus floridanus, Harpegnathus saltator, Apis mellifera, and Nasonia vitripennis.This pathway in A. cephalotes was found to be missing the two enzymes agininosuccinate synthase (EC 6.3.4.5) and argininosuccinate lyase (EC 4.3.2.1), which catalyzes the conversion of aspartate and citrulline into arginine. Other enzymes in this pathway include ornithine cabamoyltransferase (EC 2.1.3.3), arginase (EC 3.5.3.1) and nitric oxide synthase (EC 1.14.13.39). Dotted arrows indicate genes encoding proteins which were not found.
Mentions: Given the tight obligate association that A. cephalotes has with its fungal mutualist, one might predict that it acquires amino acids from its fungus in a manner similar to that of the pea aphid Acyrthosiphon pisum, which obtains amino acids from its bacterial symbionts [28]. To test this, we performed a metabolic reconstruction analysis using the Kyoto Encyclopedia of Genes and Genomes (KEGG) [69]. A. cephalotes contains a nearly identical set of amino acid biosynthesis genes as A. mellifera, C. floridanus, H. saltator, and N. vitripennis, all of which are incapable of synthesizing histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine de novo. The only exception is arginine, and only A. cephalotes was found to lack the genes necessary for its biosynthesis (Figure 3). Arginine, which is produced through the conversion of citrulline and aspartate [70], [71], is predicted to be synthesized at levels too low to support growth in insects [72].

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