1932

Abstract

Feeding on living or dead plant material is widespread in insects. Seminal work on termites and aphids has provided profound insights into the critical nutritional role that microbes play in plant-feeding insects. Some ants, beetles, and termites, among others, have evolved the ability to use microbes to gain indirect access to plant substrate through the farming of a fungus on which they feed. Recent genomic studies, including studies of insect hosts and fungal and bacterial symbionts, as well as metagenomics and proteomics, have provided important insights into plant biomass digestion across insect–fungal mutualisms. Not only do advances in understanding of the divergent and complementary functions of complex symbionts reveal the mechanism of how these herbivorous insects catabolize plant biomass, but these symbionts also represent a promising reservoir for novel carbohydrate-active enzyme discovery, which is of considerable biotechnological interest.

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2021-01-07
2024-10-09
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Literature Cited

  1. 1. 
    Aanen DK, Boomsma JJ. 2005. Evolutionary dynamics of the mutualistic symbiosis between fungus-growing termites and Termitomyces fungi. Insect-Fungal Associations: Ecology and Evolution FE Vega, M Blackwell 191–210 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  2. 2. 
    Aanen DK, Eggleton P. 2005. Fungus-growing termites originated in African rain forest. Curr. Biol. 15:9851–55
    [Google Scholar]
  3. 3. 
    Aanen DK, Eggleton P, Rouland-Lefèvre C, Guldberg-Frøslev T, Rosendahl S, Boomsma JJ 2002. The evolution of fungus-growing termites and their mutualistic fungal symbionts. PNAS 99:2314887–92
    [Google Scholar]
  4. 4. 
    Aanen DK, Ros VID, de Fine Licht HH, Mitchell J, De Beer ZW et al. 2007. Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evol. Biol. 7:115
    [Google Scholar]
  5. 5. 
    Abril AB, Bucher EH. 2002. Evidence that the fungus cultured by leaf-cutting ants does not metabolize cellulose. Ecol. Lett. 5:3325–28
    [Google Scholar]
  6. 6. 
    Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA et al. 2011. Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J 5:81323–31
    [Google Scholar]
  7. 7. 
    Aylward FO, Burnum KE, Scott JJ, Suen G, Tringe SG et al. 2012. Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens. ISME J 6:91688–701
    [Google Scholar]
  8. 8. 
    Aylward FO, Burnum-Johnson KE, Tringe SG, Teiling C, Tremmel DM et al. 2013. Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus. Appl. Environ. Microbiol. 79:123770–78
    [Google Scholar]
  9. 9. 
    Aylward FO, Khadempour L, Tremmel DM, McDonald BR, Piehowski D et al. 2015. Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants. PLOS ONE 10:9e0139151
    [Google Scholar]
  10. 10. 
    Aylward FO, Suen G, Biedermann PHW, Adams AS, Scott JJ et al. 2014. Convergent bacterial microbiotas in the fungal agricultural systems of insects. mBio 5:6e02077–14
    [Google Scholar]
  11. 11. 
    Batra LR. 1963. Ecology of ambrosia fungi and their dissemination by beetles. Trans. Kansas Acad. Sci. 66:2213–36
    [Google Scholar]
  12. 12. 
    Biedermann PHW, Vega FE. 2020. Ecology and evolution of insect-fungus mutualisms. Annu. Rev. Entomol. 65:431–55
    [Google Scholar]
  13. 13. 
    Blaz J, Barrera-Redondo J, Vázquez-Rosas-Landa M, Canedo-Téxon A, von Wobeser EA et al. 2019. Genomic signals of adaptation towards mutualism and sociality in two ambrosia beetle complexes. Life 9:1E2
    [Google Scholar]
  14. 14. 
    Book AJ, Lewin GR, McDonald BR, Takasuka TE, Doering DT et al. 2014. Cellulolytic Streptomyces strains associated with herbivorous insects share a phylogenetically linked capacity to degrade lignocellulose. Appl. Environ. Microbiol. 80:154692–701
    [Google Scholar]
  15. 15. 
    Book AJ, Lewin GR, McDonald BR, Takasuka TE, Fox G, Currie CR 2016. Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. PLOS Biol 14:6e1002475
    [Google Scholar]
  16. 16. 
    Bordeaux JM. 2008. Characterization of growth conditions for production of a laccase-like phenoloxidase by Amylostereum areolatum, a fungal pathogen of pines and other conifers M.S. thesis, Univ. Ga Athens, GA:
    [Google Scholar]
  17. 17. 
    Bot ANM, Rehner SA, Boomsma JJ 2001. Partial incompatibility between ants and symbiotic fungi in two sympatric species of Acromyrmex leaf-cutting ants. Evolution 55:101980–91
    [Google Scholar]
  18. 18. 
    Boutton TW, Arshad MA, Tieszen LL 1983. Stable isotope analysis of termite food habits in East African grasslands. Oecologia 59:11–6
    [Google Scholar]
  19. 19. 
    Branstetter MG, Ješovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC et al. 2017. Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc. R. Soc. B 284:185220170095
    [Google Scholar]
  20. 20. 
    Brune A. 2014. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12:3168–80
    [Google Scholar]
  21. 21. 
    Chapela IH, Rehner SA, Schultz TR, Mueller UG 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:51911691–94
    [Google Scholar]
  22. 22. 
    Currie CR. 2003. Ancient tripartite coevolution in the Attine ant-microbe symbiosis. Science 299:5605386–88
    [Google Scholar]
  23. 23. 
    Currie CR, Stuart AE. 2001. Weeding and grooming of pathogens in agriculture by ants. Proc. R. Soc. B 268:14711033–39
    [Google Scholar]
  24. 24. 
    da Costa RR, Hu H, Li H, Poulsen M 2019. Symbiotic plant biomass decomposition in fungus-growing termites. Insects 10:4E87
    [Google Scholar]
  25. 25. 
    da Costa RR, Hu H, Pilgaard B, Sabine SM, Schückel J et al. 2018. Enzyme activities at different stages of plant biomass decomposition in three species of fungus growing termites. Appl. Environ. Microbiol. 84:5e01815–17
    [Google Scholar]
  26. 26. 
    da Costa RR, Vreeburg SME, Shik JZ, Aanen DK, Poulsen M 2019. Can interaction specificity in the fungus-farming termite symbiosis be explained by nutritional requirements of the fungal crop. Fungal Ecol 38:54–61
    [Google Scholar]
  27. 27. 
    Dangerfield JM, Schuurman G. 2000. Foraging by fungus-growing termites (Isoptera: Termitidae, Macrotermitinae) in the Okavango Delta, Botswana. J. Trop. Ecol. 16:5717–31
    [Google Scholar]
  28. 28. 
    de Britto JS, Forti LC, de Oliveira MA, Zanetti R, Wilcken CF et al. 2016. Use of alternatives to PFOS, its salts and PFOSF for the control of leaf-cutting ants Atta and Acromyrmex.. Int. J. Res. Environ. Stud 3:11–92
    [Google Scholar]
  29. 29. 
    De Fine Licht HH, Biedermann PHW 2012. Patterns of functional enzyme activity in fungus farming ambrosia beetles. Front. Zool. 9:113
    [Google Scholar]
  30. 30. 
    De Fine Licht HH, Boomsma JJ 2010. Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecol. Entomol. 35:3259–69
    [Google Scholar]
  31. 31. 
    De Fine Licht HH, Boomsma JJ, Tunlid A 2014. Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nat. Commun. 5:5675
    [Google Scholar]
  32. 32. 
    De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P, Boomsma JJ 2013. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. PNAS 110:2583–87
    [Google Scholar]
  33. 33. 
    Dietrich C, Köhler T, Brune A 2014. The cockroach origin of the termite gut microbiota: Patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80:72261–69
    [Google Scholar]
  34. 34. 
    Douglas AE. 1994. Symbiotic Interactions Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  35. 35. 
    Eggleton P. 2000. Global patterns of termite diversity. Termites: Evolution, Sociality, Symbioses, Ecology T Abe, DE Bignell, M Higashi 25–51 Berlin: Springer
    [Google Scholar]
  36. 36. 
    Farrell BD, Sequeira AS, O'Meara BC, Normark BB, Chung JH, Jordal BH 2001. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:102011–27
    [Google Scholar]
  37. 37. 
    Fitza KNE, Tabata M, Kanzaki N, Kimura K, Garnas J, Slippers B 2016. Host specificity and diversity of Amylostereum associated with Japanese siricids. Fungal Ecol 24:76–81
    [Google Scholar]
  38. 38. 
    Fox BG, Takasuka T, Book AJ, Currie CR 2019. Method and compositions for improved lignocellulosic material hydrolysis US Patent 20130189744A1
    [Google Scholar]
  39. 39. 
    Francoeur CB, Khadempour L, Moreira-Soto RD, Gotting K, Book AJ et al. 2020. Bacteria contribute to plant secondary compound degradation in a generalist herbivore system. mBio In press
    [Google Scholar]
  40. 40. 
    Fu N, Wang M, Wang L, Luo O, Ren L 2020. Genome sequencing and analysis of the fungal symbiont of Sirex noctilio, Amylostereum areolatum: revealing the biology of fungus-insect mutualism. mSphere 5:3e00301–20
    [Google Scholar]
  41. 41. 
    Garcia MG, Forti LC, Verza SS, Noronha NC, Nagamoto NS 2005. Interference of epicuticular wax from leaves of grasses in selection and preparation of substrate for cultivation of symbiont fungus by Atta capiguara (Hym. Formicidae). Sociobiology 45:3937–47
    [Google Scholar]
  42. 42. 
    Gelfand I, Sahajpal R, Zhang X, Izaurralde RC, Gross KL, Robertson GP 2013. Sustainable bioenergy production from marginal lands in the US Midwest. Nature 493:7433514–17
    [Google Scholar]
  43. 43. 
    Grell MN, Linde T, Nygaard S, Nielsen KL, Boomsma JJ, Lange L 2013. 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 14:928
    [Google Scholar]
  44. 44. 
    Grimaldi D, Engel MS 2005. Evolution of the Insects Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  45. 45. 
    Grubbs KJ, Surup F, Bidermann PH, McDonald BR, Klassen Jet al 2020. Cyclohexamide-producing Streptomyces associated with Xyleborinus saxesenii and Xyleborus affinis fungus-farming ambrosia beetles. Front. Microbiol In press
    [Google Scholar]
  46. 46. 
    Hajek AE, Nielsen C, Kepler RM, Long SJ, Castrillo L 2013. Fidelity among Sirex woodwasps and their fungal symbionts. Microb. Ecol. 65:3753–62
    [Google Scholar]
  47. 47. 
    Hinze B, Crailsheim K, Leuthold RH 2002. Polyethism in food processing and social organisation in the nest of Macrotermes bellicosus (Isoptera, Termitidae). Insectes Soc 49:131–37
    [Google Scholar]
  48. 48. 
    Hölldobler B, Wilson E. 1990. The Ants Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  49. 49. 
    Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S et al. 2006. Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol. Ecol 15:2505–16
    [Google Scholar]
  50. 50. 
    Hu H, da Costa RR, Pilgaard B, Schiøtt M, Lange L, Poulsen M 2019. Fungiculture in termites is associated with a mycolytic gut bacterial community. mSphere 4:3e00165–19
    [Google Scholar]
  51. 51. 
    Huang Y-T, Skelton J, Hulcr J 2019. Multiple evolutionary origins lead to diversity in the metabolic profiles of ambrosia fungi. Fungal Ecol 38:80–88
    [Google Scholar]
  52. 52. 
    Huang Y-T, Skelton J, Hulcr J 2020. Lipids and small metabolites provisioned by ambrosia fungi to symbiotic beetles are phylogeny-dependent, not convergent. ISME J 14:1089–99
    [Google Scholar]
  53. 53. 
    Hughes WOH, Howse PE, Goulson D 2001. Mandibular gland chemistry of grass-cutting ants: species, caste, and colony variation. J. Chem. Ecol. 27:1109–24
    [Google Scholar]
  54. 54. 
    Hulcr J, Rountree NR, Diamond SE, Stelinski LL, Fierer N, Dunn RR 2012. Mycangia of ambrosia beetles host communities of bacteria. Microb. Ecol. 64:3784–93
    [Google Scholar]
  55. 55. 
    Hulcr J, Stelinski LL. 2017. The ambrosia symbiosis: from evolutionary ecology to practical management. Annu. Rev. Entomol. 62:285–303
    [Google Scholar]
  56. 56. 
    Hyodo F, Inoue T, Azuma J-I, Tayasu I, Abe T 2000. Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae). Soil Biol. Biochem. 32:5653–58
    [Google Scholar]
  57. 57. 
    Hyodo F, Tayasu I, Inoue T, Azuma J, Kudo T, Abe T 2003. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct. Ecol. 17:2186–93
    [Google Scholar]
  58. 58. 
    Ibarra-Juarez LA, Desgarennes D, Vázquez-Rosas-Landa M, Villafan E, Alonso-Sánchez A et al. 2018. Impact of rearing conditions on the ambrosia beetle's microbiome. Life 8:4E63
    [Google Scholar]
  59. 59. 
    Deleted in proof
  60. 60. 
    Johjima T, Taprab Y, Noparatnaraporn N, Kudo T, Ohkuma M 2006. Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl. Microbiol. Biotechnol. 73:1195–203
    [Google Scholar]
  61. 61. 
    Johnson RA, Thomas RJ, Wood TG, Swift MJ 1981. The inoculation of the fungus comb in newly founded colonies of some species of the Macrotermitinae (Isoptera) from Nigeria. J. Nat. Hist. 15:5751–56
    [Google Scholar]
  62. 62. 
    Kallio P, Pásztor A, Akhtar MK, Jones PR 2014. Renewable jet fuel. Curr. Opin. Biotechnol. 26:50–55
    [Google Scholar]
  63. 63. 
    Kasson MT, Wickert KL, Stauder CM, Macias AM, Berger MC et al. 2016. Mutualism with aggressive wood-degrading Flavodon ambrosius (Polyporales) facilitates niche expansion and communal social structure in Ambrosiophilus ambrosia beetles. Fungal Ecol 23:86–96
    [Google Scholar]
  64. 64. 
    Khadempour L, Burnum-Johnson EK, Baker ES, Nicora CD, Webb-Robertson B-JM et al. 2016. The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates. Mol. Ecol. 25:225795–805
    [Google Scholar]
  65. 65. 
    Kircher M. 2015. Sustainability of biofuels and renewable chemicals production from biomass. Curr. Opin. Chem. Biol. 29:26–31
    [Google Scholar]
  66. 66. 
    Kirkendall LR, Biedermann PHW, Jordal BH 2015. Evolution and diversity of bark and ambrosia beetles. Bark Beetles: Biology and Ecology of Native and Invasive Species FE Vega, RW Hofstetter 85–156 New York: Acad. Press
    [Google Scholar]
  67. 67. 
    Kok LT, Norris DM, Chu HM 1970. Sterol metabolism as a basis for a mutualistic symbiosis. Nature 225:5233661–62
    [Google Scholar]
  68. 68. 
    Kooij PW, Pullens JWM, Boomsma JJ, Schiøtt M 2016. Ant mediated redistribution of a xyloglucanase enzyme in fungus gardens of Acromyrmex echinatior. BMC Microbiol 16:81
    [Google Scholar]
  69. 69. 
    Kooij PW, Rogowska-Wrzesinska A, Hoffmann D, Roepstorff P, Boomsma JJ, Schiøtt M 2014. Leucoagaricus gongylophorus uses leaf-cutting ants to vector proteolytic enzymes towards new plant substrate. ISME J 8:51032–40
    [Google Scholar]
  70. 70. 
    Korb J, Aanen DK. 2003. The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae). Behav. Ecol. Sociobiol. 53:265–71
    [Google Scholar]
  71. 71. 
    Kostovcik M, Bateman CC, Kolarik M, Stelinski LL, Jordal BH, Hulcr J 2015. The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J 9:1126–38
    [Google Scholar]
  72. 72. 
    Kukor JJ, Martin MM. 1983. Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont. Science 220:46021161–63
    [Google Scholar]
  73. 73. 
    Leal IR, Oliveira PS. 2000. Foraging ecology of attine ants in a Neotropical savanna: seasonal use of fungal substrate in the cerrado vegetation of Brazil. Insectes Soc 47:4376–82
    [Google Scholar]
  74. 74. 
    Lewin GR, Johnson AL, Soto RDM, Perry K, Book AJ et al. 2016. Cellulose-enriched microbial communities from leaf-cutter ant (Atta colombica) refuse dumps vary in taxonomic composition and degradation ability. PLOS ONE 11:3e0151840
    [Google Scholar]
  75. 75. 
    Li D, Shi J, Lu M, Ren L, Zhen C, Luo Y 2015. Detection and identification of the invasive Sirex noctilio (Hymenoptera: Siricidae) fungal symbiont, Amylostereum areolatum (Russulales: Amylostereacea), in China and the stimulating effect of insect venom on laccase production by A. areolatum YQL03. J. Econ. Entomol. 108:31136–47
    [Google Scholar]
  76. 76. 
    Li H, Dietrich C, Zhu N, Mikaelyan A, Ma B et al. 2016. Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus. Environ. Microbiol 18:51440–51
    [Google Scholar]
  77. 77. 
    Li H, Lu J, Mo J 2012. Physiochemical lignocellulose modification by the formosan subterranean termite. BioResources 7:675–85
    [Google Scholar]
  78. 78. 
    Li H, Sosa-Calvo J, Horn HA, Pupo MT, Clardy J et al. 2018. Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. PNAS 115:4210720–25
    [Google Scholar]
  79. 79. 
    Li H, Yang M, Chen Y, Zhu N, Lee C et al. 2015. Investigation of age polyethism in food processing of the fungus-growing termite Odontotermes formosanus (Blattodea: Termitidae) using a laboratory artificial rearing system. J. Econ. Entomol. 108:266–73
    [Google Scholar]
  80. 80. 
    Li H, Yelle DJ, Li C, Yang M, Ke J et al. 2017. Lignocellulose pretreatment in a fungus-cultivating termite. PNAS 114:184709–14
    [Google Scholar]
  81. 81. 
    Li Y, Bateman CC, Skelton J, Jusino MA, Nolen ZJ et al. 2017. Wood decay fungus Flavodon ambrosius (Basidiomycota: Polyporales) is widely farmed by two genera of ambrosia beetles. Fungal Biol 121:11984–89
    [Google Scholar]
  82. 82. 
    Liang S, Wang C, Ahmad F, Yin X, Hu Y, Mo J 2020. Exploring the effect of plant substrates on bacterial community structure in termite fungus-combs. PLOS ONE 15:5e0232329
    [Google Scholar]
  83. 83. 
    Lim S, Chundawat SPS, Fox BG 2014. Expression, purification and characterization of a functional carbohydrate-binding module from Streptomyces sp. SirexAA-E. Protein Expr. Purif. 98:1–9
    [Google Scholar]
  84. 84. 
    Liu N, Zhang L, Zhou H, Zhang M, Yan X et al. 2013. Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLOS ONE 8:7e69184
    [Google Scholar]
  85. 85. 
    Madden JL. 1975. Bacteria and yeasts associated with Sirex noctilio. J. Invertebr. Pathol 25:3283–87
    [Google Scholar]
  86. 86. 
    Madden JL. 1981. Egg and larval development in the woodwasp, Sirex noctilio F. Aust. J. Zool. 29:4493–506
    [Google Scholar]
  87. 87. 
    Mayers CG, Bateman CC, Harrington TC 2018. New Meredithiella species from mycangia of Corthylus ambrosia beetles suggest genus-level coadaptation but not species-level coevolution. Mycologia 110:163–78
    [Google Scholar]
  88. 88. 
    Meirelles LA, McFrederick QS, Rodrigues A, Mantovani JD, de Melo Rodovalho C et al. 2016. Bacterial microbiomes from vertically transmitted fungal inocula of the leaf-cutting ant Atta texana. Environ. Microbiol. Rep 8:5630–40
    [Google Scholar]
  89. 89. 
    Mikaelyan A, Dietrich C, Köhler T, Poulsen M, Sillam-Dussès D, Brune A 2015. Diet is the primary determinant of bacterial community structure in the guts of higher termites. Mol. Ecol. 24:205284–95
    [Google Scholar]
  90. 90. 
    Moreira-Soto RD, Sanchez E, Currie CR, Pinto-Tomás AA 2017. Ultrastructural and microbial analyses of cellulose degradation in leaf-cutter ant colonies. Microbiology 163:111578–89
    [Google Scholar]
  91. 91. 
    Mueller UG, Gerardo N. 2002. Fungus-farming insects: multiple origins and diverse evolutionary histories. PNAS 99:2415247–49
    [Google Scholar]
  92. 92. 
    Munkacsi AB, Pan JJ, Villesen P, Mueller UG, Blackwell M, McLaughlin DJ 2004. Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants. Proc. R. Soc. Lond. B 271:15501777–82
    [Google Scholar]
  93. 93. 
    Nagamoto NS, Garcia MG, Forti LC, Verza SS, Noronha NC, Rodella RA 2011. Microscopic evidence supports the hypothesis of high cellulose degradation capacity by the symbiotic fungus of leaf-cutting ants. J. Biol. Res. 16:308–12
    [Google Scholar]
  94. 94. 
    Nobre T, Koné NA, West R, Hubland A 2011. Dating the fungus-growing termites’ mutualism shows a mixture between ancient codiversification and recent symbiont dispersal across divergent hosts. Mol. Ecol. 20:2619–27
    [Google Scholar]
  95. 95. 
    Nygaard S, Hu H, Li C, Schiøtt M, Chen Z et al. 2016. Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. Nat. Commun. 7:12233
    [Google Scholar]
  96. 96. 
    Ohkuma M. 2003. Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl. Microbiol. Biotechnol. 61:11–9
    [Google Scholar]
  97. 97. 
    Otani S, Hansen LH, Sørensen SJ, Poulsen M 2016. Bacterial communities in termite fungus combs are comprised of consistent gut deposits and contributions from the environment. Microb. Ecol. 71:1207–20
    [Google Scholar]
  98. 98. 
    Otani S, Mikaelyan A, Nobre T, Hansen LH, Koné NA et al. 2014. Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23:184631–44
    [Google Scholar]
  99. 99. 
    Otani S, Zhukova M, Koné NA, da Costa RR, Mikaelyan A et al. 2019. Gut microbial compositions mirror caste-specific diets in a major lineage of social insects. Environ. Microbiol. Rep. 11:2196–205
    [Google Scholar]
  100. 100. 
    Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST et al. 2009. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:59561120–23
    [Google Scholar]
  101. 101. 
    Poulsen M, Hu H, Li C, Chen Z, Xu L et al. 2014. Complementary symbiont contributions to plant decomposition in a fungus-farming termite. PNAS 111:4014500–5
    [Google Scholar]
  102. 102. 
    Ranger CM, Reding ME, Schultz PB, Oliver JB, Frank SD et al. 2016. Biology, ecology, and management of nonnative ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) in ornamental plant nurseries. J. Integr. Pest Manag. 7:19
    [Google Scholar]
  103. 103. 
    Rønhede S, Boomsma JJ, Rosendahl S 2004. Fungal enzymes transferred by leaf-cutting ants in their fungus gardens. Mycol. Res. 108:1101–6
    [Google Scholar]
  104. 104. 
    Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI 2004. Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol. Lett 239:2319–23
    [Google Scholar]
  105. 105. 
    Sapountzis P, de Verges J, Rousk K, Cilliers M, Vorster BJ, Poulsen M 2016. Potential for nitrogen fixation in the fungus-growing termite symbiosis. Front. Microbiol. 7:1993
    [Google Scholar]
  106. 106. 
    Sapountzis P, Nash DR, Schiøtt M, Boomsma JJ 2019. The evolution of abdominal microbiomes in fungus-growing ants. Mol. Ecol. 28:4879–99
    [Google Scholar]
  107. 107. 
    Schiøtt M, De Fine Licht HH, Lange L, Boomsma JJ 2008. 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 8:40
    [Google Scholar]
  108. 108. 
    Schiøtt M, Rogowska-Wrzesinska A, Roepstorff P, Boomsma JJ 2010. Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi. BMC Biol 8:1156
    [Google Scholar]
  109. 109. 
    Schultz TR, Brady SG. 2008. Major evolutionary transitions in ant agriculture. PNAS 105:145435–40
    [Google Scholar]
  110. 110. 
    Scott JJ, Budsberg KJ, Suen G, Wixon DL, Balser TC, Currie CR 2010. Microbial community structure of leaf-cutter ant fungus gardens and refuse dumps. PLOS ONE 5:3e9922
    [Google Scholar]
  111. 111. 
    Shik JZ, Gomez EB, Kooij PW, Santos JC, Wcislo WT, Boomsma JJ 2016. Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant. PNAS 113:3610121–26
    [Google Scholar]
  112. 112. 
    Shik JZ, Rytter W, Arnan X, Michelsen A 2018. Disentangling nutritional pathways linking leafcutter ants and their co-evolved fungal symbionts using stable isotopes. Ecology 99:91999–2009
    [Google Scholar]
  113. 113. 
    Sieber R, Leuthold RH. 1981. Behavioural elements and their meaning in incipient laboratory colonies of the fungus-growing termite Macrotermes michaelseni (Isoptera: Macrotermitinae). Insectes Soc 28:4371–82
    [Google Scholar]
  114. 114. 
    Sinotte VM, Renelies-Hamilton J, Taylor BA, Ellegaard KM, Sapountzis P, Vasseur-Cognet M 2020. Synergies between division of labor and gut microbiomes of social insects. Front. Ecol. Evol. 7:503
    [Google Scholar]
  115. 115. 
    Skelton J, Johnson AJ, Jusino MA, Bateman CC, Li Y, Hulcr J 2019. A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts. Proc. R. Soc. B 286:20182127
    [Google Scholar]
  116. 116. 
    Slippers B, Coutinho TA, Wingfield BD, Wingfield MJ 2003. A review of the genus Amylostereum and its association with woodwasps. S. Afr. J. Sci. 99:1–270–74
    [Google Scholar]
  117. 117. 
    Slippers B, Wingfield MJ, Wingfield BD, Coutinho TA 2000. Relationships among Amylostereum species associated with siricid woodwasps inferred from mitochondrial ribosomal DNA sequences. Mycologia 92:5955–63
    [Google Scholar]
  118. 118. 
    Solomon SE, Rabeling C, Sosa-Calvo J, Lopes CT, Rodrigues A et al. 2019. The molecular phylogenetics of Trachymyrmex forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of “higher-attine” ant agriculture. Syst. Entomol. 44:4939–56
    [Google Scholar]
  119. 119. 
    Somera AF, Lima AM, Dos Santos-Neto ÁJ, Lanças FM, Bacci M 2015. Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications. Appl. Environ. Microbiol. 81:134525–35
    [Google Scholar]
  120. 120. 
    Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG et al. 2010. An insect herbivore microbiome with high plant biomass-degrading capacity. PLOS Genet 6:9e1001129
    [Google Scholar]
  121. 121. 
    Suen G, Teiling C, Li L, Holt C, Abouheif E et al. 2011. The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLOS Genet 7:2e1002007
    [Google Scholar]
  122. 122. 
    Takasuka TE, Book AJ, Lewin GR, Currie CR, Fox BG 2013. Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces. Sci. Rep 3:1030
    [Google Scholar]
  123. 123. 
    Tarno H, Septia ED, Aini LQ 2016. Microbial community associated with ambrosia beetle, Euplatypus parallelus on Sonokembang, Pterocarpus indicus in Malang. AGRIVITA J. Agric. Sci 38:3312–20
    [Google Scholar]
  124. 124. 
    Thompson BM, Grebenok RJ, Behmer ST, Gruner DS 2013. Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp. Sirex noctilio. J. Chem. Ecol. 39:1129–39
    [Google Scholar]
  125. 125. 
    Thomsen IM, Koch J. 1999. Somatic compatibility in Amylostereum areolatum and A. chailletii as a consequence of symbiosis with siricid woodwasps. Mycol. Res. 103:7817–23
    [Google Scholar]
  126. 126. 
    Um S, Fraimout A, Sapountzis P, Oh D-C, Poulsen M 2013. The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi. Sci. Rep. 3:3250
    [Google Scholar]
  127. 127. 
    van de Peppel LJJ, Aanen DK 2020. High diversity and low host-specificity of Termitomyces symbionts cultivated by Microtermes spp. indicate frequent symbiont exchange. Fungal Ecol 45:100917
    [Google Scholar]
  128. 128. 
    Vanderpool D, Bracewell RR, McCutcheon JP 2018. Know your farmer: ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars. Mol. Ecol. 27:82077–94
    [Google Scholar]
  129. 129. 
    Vasiliauskas R, Stenlid J, Thomsen IM 1998. Clonality and genetic variation in Amylostereum areolatum and A. chailletii from northern Europe. New Phytol 139:4751–58
    [Google Scholar]
  130. 130. 
    Visser AA, Nobre T, Currie CR, Aanen DK, Poulsen M 2012. Exploring the potential for Actinobacteria as defensive symbionts in fungus-growing termites. Microb. Ecol. 63:4975–85
    [Google Scholar]
  131. 131. 
    Watanabe H, Tokuda G. 2010. Cellulolytic systems in insects. Annu. Rev. Entomol. 55:609–32
    [Google Scholar]
  132. 132. 
    Weber NA. 1972. Gardening Ants: The Attines Philadelphia, PA: Am. Phil. Soc.
    [Google Scholar]
  133. 133. 
    Wirth R, Herz H, Ryel RJ, Beyschlag W, Hölldobler B 2003. Herbivory of Leaf-Cutting Ants: A Case Study on Atta colombica in the Tropical Rain Forest of Panama Berlin: Springer
    [Google Scholar]
  134. 134. 
    Wood TG, Sands WA, Brian MV 1978. Production Ecology of Ants and Termites Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  135. 134a. 
    Worsley SF, Innocent TM, Heine D, Murrell CJ, Yu DWet al 2018. Symbiotic partnerships and their chemical interactions in the leafcutter ants (Hymenoptera: Formicidae). Myrmecol. News 27:59–74
    [Google Scholar]
  136. 135. 
    Zhukova M, Sapountzis P, Schiøtt M, Boomsma JJ 2017. Diversity and transmission of gut bacteria in Atta and Acromyrmex leaf-cutting ants during development. Front. Microbiol. 8:1942
    [Google Scholar]
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