The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Grell, Morten N ^a   Linde, Tore ^a,b   Nygaard, Sanne ^b   Nielsen, Kåre L ^a   Boomsma, Jacobus J ^b   Lange, Lene ^a  

^a AALBORG UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Acromyrmex echinatior; Attine ants; Biomass conversion; Carbohydrate active enzymes (CAZymes); DeepSAGE; Fungus garden; Leucocoprinus gongylophorus; Symbiosis; Transcript profiling

Indexed keywords

CELLULOSE; HEMICELLULOSE; PECTIN; POLYSACCHARIDE;

ACROMYRMEX ECHINATIOR; ANT; ARTICLE; BIOMASS CONVERSION; CARBOHYDRATE METABOLISM; DECOMPOSITION; DEGRADATION; FUNGUS; FUNGUS HYPHAE; GENE EXPRESSION; GENETIC TRANSCRIPTION; MYCELIUM; NONHUMAN; NUTRIENT; PLANT CELL; SYMBIONT;

ACROMYRMEX; ACROMYRMEX ECHINATIOR; ATTA; FORMICIDAE; FUNGI; LEUCOCOPRINUS;

AGARICALES; ANIMALS; ANTS; BIOMASS; CELL WALL; CELLULASES; CELLULOSE; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION, FUNGAL; GENE LIBRARY; GENES, FUNGAL; POLYSACCHARIDES; SYMBIOSIS;

EID: 84890966935     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-928     Document Type: Article

References (49)

1. Schultz TR, Brady SG. Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 2008, 105:5435-5440. 10.1073/pnas.0711024105, 2291119, 18362345.
2. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung G, Spatafora JW, Straus NA. Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 2003, 299:386-388. 10.1126/science.1078155, 12532015.
3. Mueller UG, Schultz TR, Currie CR, Adams RMM, Malloch D. The origin of the attine ant-fungus mutualism. Q Rev Biol 2001, 76:169-197. 10.1086/393867, 11409051.
4. Chapela IH, Rehner SA, Schultz TR, Mueller UG. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 1994, 266:1691-1694. 10.1126/science.266.5191.1691, 17775630.
5. Currie CR. A Community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 2001, 55:357. 10.1146/annurev.micro.55.1.357, 11544360.
6. De Fine Licht HH, Boomsma JJ. Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecol Entomol 2010, 35:259-269.
7. Schiøtt M, Rogowska-Wrzesinska A, Roepstorff P, Boomsma JJ. Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi. BMC Biol 2010, 8:156. 10.1186/1741-7007-8-156, 3022778, 21194476.
8. De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P, Boomsma JJ. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proc Natl Acad Sci USA 2013, 110:583-587. 10.1073/pnas.1212709110, 3545816, 23267060.
9. Rønhede S, Boomsma JJ, Rosendahl S. Fungal enzymes transferred by leaf-cutting ants in their fungus gardens. Mycol Res 2004, 108:101-106. 10.1017/S0953756203008931, 15035511.
10. Moller IE, De Fine Licht HH, Harholt J, Willats WGT, Boomsma JJ. The dynamics of plant cell-wall polysaccharide decomposition in leaf-cutting ant fungus gardens. PLoS One 2011, 6:e17506. 10.1371/journal.pone.0017506, 3053354, 21423735.
11. Weber NA. Fungus-growing ants. Science 1966, 153:587-604. 10.1126/science.153.3736.587, 17757227.
12. Quinlan RJ, Cherrett JM. The role of fungus in the diet of the leaf-cutting ant Atta cephalotes (L.). Ecol Entomol 1979, 4:151-160.
13. Boyd ND, Martin MM. Faecal proteinases of the fungus-growing ant, Atta texana: their fungal origin and ecological significance. J Insect Physiol 1975, 21:1815-1820.
14. Aylward FO, Currie CR, Suen G. The evolutionary innovation of nutritional symbioses in leaf-cutter ants. Insects 2012, 3:41-61.
15. Schiøtt M, De Fine Licht HH, Lange L, Boomsma JJ. Towards a molecular understanding of symbiont function: identification of a fungal gene for the degradation of xylan in the fungus gardens of leaf-cutting ants. BMC Microbiol 2008, 8:40. 10.1186/1471-2180-8-40, 2291056, 18307762.
16. de Siqueira CG, Bacci M, Pagnocca FC, Bueno OC, Hebling MJA. Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L. Appl Environ Microbiol 1998, 64:4820-4822. 90928, 9835568.
17. De Fine Licht HH, Schiøtt M, Mueller UG, Boomsma JJ. Evolutionary transitions in enzyme activity of ant fungus gardens. Evolution 2010, 64:2055-2069.
18. Erthal M, Silva CP, Cooper RM, Samuels RI. Hydrolytic enzymes of leaf-cutting ant fungi. Comp Biochem Physiol B Biochem Mol Biol 2009, 152:54-59. 10.1016/j.cbpb.2008.09.086, 18848636.
19. Abril AB, Bucher EH. Evidence that the fungus cultured by leaf-cutting ants does not metabolize cellulose. Ecol Lett 2002, 5:325-328.
20. Abril AB, Bucher EH. Nutritional sources of the fungus cultured by leaf-cutting ants. Appl Soil Ecol 2004, 26:243-247.
21. Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG, Pinto-Tomas AA, Foster CE, Pauly M, Weimer PJ, Barry KW, Goodwin LA, Bouffard P, Li L, Osterberger J, Harkins TT, Slater SC, Donohue TJ, Currie CR. An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet 2010, 6:e1001129. 10.1371/journal.pgen.1001129, 2944797, 20885794.
22. Nagamoto NS, Garcia MG, Forti LC, Verza SS, Noronha NC, Rodella RA. Microscopic evidence supports the hypothesis of high cellulose degradation capacity by the symbiotic fungus of leaf-cutting ants. J Biol Res-Thessalon 2011, 16:308-312.
23. Baldrian P, Valášková V. Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 2008, 32:501-521. 10.1111/j.1574-6976.2008.00106.x, 18371173.
24. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, De Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, et al. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 2012, 336:1715-1719. 10.1126/science.1221748, 22745431.
25. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VGH. Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 2012, 5:45. 10.1186/1754-6834-5-45, 3492096, 22747961.
26. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238. 10.1093/nar/gkn663, 2686590, 18838391.
27. The carbohydrate-active enzymes database http://www.cazy.org/.
28. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 2013, 6:41. 10.1186/1754-6834-6-41, 3620520, 23514094.
29. Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 2004, 22:695-700. 10.1038/nbt967, 15122302.
30. Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagye LG, Ohm RA, Patyshakuliyeva A, Brun A, Aerts AL, Bailey AM, Billette C, Coutinho PM, Deakin G, Doddapaneni H, Floudas D, Grimwood J, Hildén K, Kües U, LaButti KM, Lapidus A, Lindquist EA, Lucas SM, Murat C, Riley RW, Salamov AA, Schmutz J, Subramanian V, Wösten HAB, Xu J, Eastwood DC, Foster GD, Sonnenberg ASM, Cullen D, de Vries RP, Lundell T, Hibbett DS, Henrissat B, Burton KS, Kerrigan RW, Challen MP, Grigoriev IV, Martin F. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci USA 2012, 109:17501-17506. 10.1073/pnas.1206847109, 3491501, 23045686.
31. Hilden L, Johansson G. Recent developments on cellulases and carbohydrate-binding modules with cellulose affinity. Biotechnol Lett 2004, 26:1683-1693. 10.1007/s10529-004-4579-8, 15604820.
32. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 2004, 382:769-781. 10.1042/BJ20040892, 1133952, 15214846.
33. Nielsen KL, Høgh AL, Emmersen J. DeepSAGE-digital transcriptomics with high sensitivity, simple experimental protocol and multiplexing of samples. Nucleic Acids Res 2006, 34:e133. 10.1093/nar/gkl714, 1636492, 17028099.
34. Basic local alignment search tool http://blast.ncbi.nlm.nih.gov/Blast.cgi.
35. Busk PK, Lange L. Function-based classification of carbohydrate-active enzymes by recognition of short, conserved peptide motifs. Appl Environ Microbiol 2013, 79:3380-3391. 10.1128/AEM.03803-12, 3648057, 23524681.
36. Pazzagli L, Zoppi C, Carresi L, Tiribilli B, Sbrana F, Schiff S, Pertinhez TA, Scala A, Cappugi G. Characterization of ordered aggregates of cerato-platanin and their involvement in fungus-host interactions. Biochim Biophys Acta-Gen Subj 2009, 1790:1334-1344.
37. Aylward FO, Burnum-Johnson KE, Tringe SG, Teiling C, Tremmel DM, Moeller JA, Scott JJ, Barry KW, Piehowski PD, Nicora CD, Malfatti SA, Monroe ME, Purvine SO, Goodwin LA, Smith RD, Weinstock GM, Gerardo NM, Suen G, Lipton MS, Currie CR. Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens. Appl Environ Microbiol 2013, 79:3770-3778. 10.1128/AEM.03833-12, 3675943, 23584789.
38. Yakovlev I, Vaaje-Kolstad G, Hietala AM, Stefanczyk E, Solheim H, Fossdal CG. Substrate-specific transcription of the enigmatic GH61 family of the pathogenic white-rot fungus Heterobasidion irregulare during growth on lignocellulose. Appl Microbiol Biotechnol 2012, 95:979-990. 10.1007/s00253-012-4206-x, 3405238, 22718248.
39. Rineau F, Roth D, Shah F, Smits M, Johansson T, Canback B, Olsen PB, Persson P, Grell MN, Lindquist E, Grigoriev IV, Lange L, Tunlid A. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ Microbiol 2012, 14:1477-1487. 10.1111/j.1462-2920.2012.02736.x, 3440587, 22469289.
40. Silva A, Bacci M, de Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJA. Survival of Atta sexdens workers on different food sources. J Insect Physiol 2003, 49:307-313. 10.1016/S0022-1910(03)00004-0, 12769984.
41. Silva A, Bacci M, Pagnocca FC, Bueno OC, Hebling MJA. Production of polysaccharidases in different carbon sources by Leucoagaricus gongylophorus Möller (Singer), the symbiotic fungus of the leaf-cutting ant Atta sexdens Linnaeus. Curr Microbiol 2006, 53:68-71. 10.1007/s00284-005-0431-1, 16775790.
42. Bacci M, Anversa MM, Pagnocca FC. Cellulose degradation by Leucocoprinus gongylophorus, the fungus cultured by the leaf-cutting ant Atta sexdens rubropilosa. Anton Leeuw Int J G 1995, 67:385-386.
43. Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST, Cleland WW, Weimer PJ, Currie CR. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 2009, 326:1120-1123. 10.1126/science.1173036, 19965433.
44. Currie CR, Scott JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999, 398:701-704.
45. Bot ANM, Boomsma JJ. Variable metapleural gland size-allometries in Acromyrmex leafcutter ants (Hymenoptera: Formicidae). J Kans Entomol Soc 1996, 69:375-383.
46. Nielsen KL. DeepSAGE: higher sensitivity and multiplexing of samples using a simpler experimental protocol. Meth Mol Biol 2008, 387:81-94.
47. Mortensen SA, Sønderkær M, Lynggaard C, Grasser M, Nielsen KL, Grasser KD. Reduced expression of the DOG1 gene in Arabidopsis mutant seeds lacking the transcript elongation factor TFIIS. FEBS Lett 2011, 585:1929-1933. 10.1016/j.febslet.2011.04.077, 21569772.
48. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829. 10.1101/gr.074492.107, 2336801, 18349386.
49. Andersen PK, Skovgaard LT. Regression with linear predictors 2010, New York: Springer.