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

Garret Suen, Clotilde Teiling, Lewyn Li, Carson Holt, Ehab Abouheif, Erich Bornberg-Bauer, Pascal Bouffard, Eric J. Caldera, Elizabeth Cash, Amy Cavanaugh, Olgert Denas, Eran Elhaik, Marie Julie Favé, Juergen Gadau, Joshua D. Gibson, Dan Graur, Kirk J. Grubbs, Darren E. Hagen, Timothy T. Harkins, Martin Helmkampf & 29 others Hao Hu, Brian R. Johnson, Jay Kim, Sarah E. Marsh, Joseph A. Moeller, Mónica C. Muñoz-TorresMó, Marguerite C. Murphy, Meredith C. Naughton, Surabhi Nigam, Rick Overson, Rajendhran Rajakumar, Justin T. Reese, Jarrod J. Scott, Chris R. Smith, Shu Tao, Neil D. Tsutsui, Lumi Viljakainen, Lothar Wissler, Mark D. Yandell, Fabian Zimmer, James Taylor, Steven C. Slater, Sandra W. Clifton, Wesley C. Warren, Christine G. Elsik, Christopher D. Smith, George M. Weinstock, Nicole M. Gerardo, Cameron R. Currie

Research output: Contribution to journalArticle

165 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere1002007
JournalPLoS Genetics
Volume7
Issue number2
DOIs
StatePublished - Feb 2011

Fingerprint

Atta cephalotes
cutters
Ants
lifestyle
ant
Life Style
Formicidae
genome
Genome
Fungi
fungus
Symbiosis
fungi
leaves
Insects
symbiosis
insect
Food
nutrients
hexamerins

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

Suen, G., Teiling, C., Li, L., Holt, C., Abouheif, E., Bornberg-Bauer, E., ... Currie, C. R. (2011). The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics, 7(2), [e1002007]. https://doi.org/10.1371/journal.pgen.1002007

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. / Suen, Garret; Teiling, Clotilde; Li, Lewyn; Holt, Carson; Abouheif, Ehab; Bornberg-Bauer, Erich; Bouffard, Pascal; Caldera, Eric J.; Cash, Elizabeth; Cavanaugh, Amy; Denas, Olgert; Elhaik, Eran; Favé, Marie Julie; Gadau, Juergen; Gibson, Joshua D.; Graur, Dan; Grubbs, Kirk J.; Hagen, Darren E.; Harkins, Timothy T.; Helmkampf, Martin; Hu, Hao; Johnson, Brian R.; Kim, Jay; Marsh, Sarah E.; Moeller, Joseph A.; Muñoz-TorresMó, Mónica C.; Murphy, Marguerite C.; Naughton, Meredith C.; Nigam, Surabhi; Overson, Rick; Rajakumar, Rajendhran; Reese, Justin T.; Scott, Jarrod J.; Smith, Chris R.; Tao, Shu; Tsutsui, Neil D.; Viljakainen, Lumi; Wissler, Lothar; Yandell, Mark D.; Zimmer, Fabian; Taylor, James; Slater, Steven C.; Clifton, Sandra W.; Warren, Wesley C.; Elsik, Christine G.; Smith, Christopher D.; Weinstock, George M.; Gerardo, Nicole M.; Currie, Cameron R.

In: PLoS Genetics, Vol. 7, No. 2, e1002007, 02.2011.

Research output: Contribution to journalArticle

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-TorresMó, 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 2011, 'The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle', PLoS Genetics, vol. 7, no. 2, e1002007. https://doi.org/10.1371/journal.pgen.1002007
Suen, Garret ; Teiling, Clotilde ; Li, Lewyn ; Holt, Carson ; Abouheif, Ehab ; Bornberg-Bauer, Erich ; Bouffard, Pascal ; Caldera, Eric J. ; Cash, Elizabeth ; Cavanaugh, Amy ; Denas, Olgert ; Elhaik, Eran ; Favé, Marie Julie ; Gadau, Juergen ; Gibson, Joshua D. ; Graur, Dan ; Grubbs, Kirk J. ; Hagen, Darren E. ; Harkins, Timothy T. ; Helmkampf, Martin ; Hu, Hao ; Johnson, Brian R. ; Kim, Jay ; Marsh, Sarah E. ; Moeller, Joseph A. ; Muñoz-TorresMó, Mónica C. ; Murphy, Marguerite C. ; Naughton, Meredith C. ; Nigam, Surabhi ; Overson, Rick ; Rajakumar, Rajendhran ; Reese, Justin T. ; Scott, Jarrod J. ; Smith, Chris R. ; Tao, Shu ; Tsutsui, Neil D. ; Viljakainen, Lumi ; Wissler, Lothar ; Yandell, Mark D. ; Zimmer, Fabian ; Taylor, James ; Slater, Steven C. ; Clifton, Sandra W. ; Warren, Wesley C. ; Elsik, Christine G. ; Smith, Christopher D. ; Weinstock, George M. ; Gerardo, Nicole M. ; Currie, Cameron R. / The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. In: PLoS Genetics. 2011 ; Vol. 7, No. 2.
@article{78a5023a763a478e8f6c51ffd713a01c,
title = "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.",
author = "Garret Suen and Clotilde Teiling and Lewyn Li and Carson Holt and Ehab Abouheif and Erich Bornberg-Bauer and Pascal Bouffard and Caldera, {Eric J.} and Elizabeth Cash and Amy Cavanaugh and Olgert Denas and Eran Elhaik and Fav{\'e}, {Marie Julie} and Juergen Gadau and Gibson, {Joshua D.} and Dan Graur and Grubbs, {Kirk J.} and Hagen, {Darren E.} and Harkins, {Timothy T.} and Martin Helmkampf and Hao Hu and Johnson, {Brian R.} and Jay Kim and Marsh, {Sarah E.} and Moeller, {Joseph A.} and Mu{\~n}oz-TorresM{\'o}, {M{\'o}nica C.} and Murphy, {Marguerite C.} and Naughton, {Meredith C.} and Surabhi Nigam and Rick Overson and Rajendhran Rajakumar and Reese, {Justin T.} and Scott, {Jarrod J.} and Smith, {Chris R.} and Shu Tao and Tsutsui, {Neil D.} and Lumi Viljakainen and Lothar Wissler and Yandell, {Mark D.} and Fabian Zimmer and James Taylor and Slater, {Steven C.} and Clifton, {Sandra W.} and Warren, {Wesley C.} and Elsik, {Christine G.} and Smith, {Christopher D.} and Weinstock, {George M.} and Gerardo, {Nicole M.} and Currie, {Cameron R.}",
year = "2011",
month = "2",
doi = "10.1371/journal.pgen.1002007",
language = "English (US)",
volume = "7",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle

AU - Suen, Garret

AU - Teiling, Clotilde

AU - Li, Lewyn

AU - Holt, Carson

AU - Abouheif, Ehab

AU - Bornberg-Bauer, Erich

AU - Bouffard, Pascal

AU - Caldera, Eric J.

AU - Cash, Elizabeth

AU - Cavanaugh, Amy

AU - Denas, Olgert

AU - Elhaik, Eran

AU - Favé, Marie Julie

AU - Gadau, Juergen

AU - Gibson, Joshua D.

AU - Graur, Dan

AU - Grubbs, Kirk J.

AU - Hagen, Darren E.

AU - Harkins, Timothy T.

AU - Helmkampf, Martin

AU - Hu, Hao

AU - Johnson, Brian R.

AU - Kim, Jay

AU - Marsh, Sarah E.

AU - Moeller, Joseph A.

AU - Muñoz-TorresMó, Mónica C.

AU - Murphy, Marguerite C.

AU - Naughton, Meredith C.

AU - Nigam, Surabhi

AU - Overson, Rick

AU - Rajakumar, Rajendhran

AU - Reese, Justin T.

AU - Scott, Jarrod J.

AU - Smith, Chris R.

AU - Tao, Shu

AU - Tsutsui, Neil D.

AU - Viljakainen, Lumi

AU - Wissler, Lothar

AU - Yandell, Mark D.

AU - Zimmer, Fabian

AU - Taylor, James

AU - Slater, Steven C.

AU - Clifton, Sandra W.

AU - Warren, Wesley C.

AU - Elsik, Christine G.

AU - Smith, Christopher D.

AU - Weinstock, George M.

AU - Gerardo, Nicole M.

AU - Currie, Cameron R.

PY - 2011/2

Y1 - 2011/2

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=79952270451&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79952270451&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1002007

DO - 10.1371/journal.pgen.1002007

M3 - Article

VL - 7

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 2

M1 - e1002007

ER -