Skip to main content
SpringerLink
Log in

Uncovering the Yeast Communities in Fungus-Growing Ant Colonies

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Yeast-insect interactions are compelling models to study the evolution, ecology, and diversification of yeasts. Fungus-growing (attine) ants are prominent insects in the Neotropics that evolved an ancient fungiculture of basidiomycete fungi over 55–65 million years, supplying an environment for a hidden yeast diversity. Here we assessed the yeast diversity in the attine ant environment by thoroughly sampling fungus gardens across four out of five ant fungiculture systems: Acromyrmex coronatus and Mycetomoellerius tucumanus standing for leaf-cutting and higher-attine fungicultures, respectively; Apterostigma sp., Mycetophylax sp., and Mycocepurus goeldii as ants from the lower-attine fungiculture. Among the fungus gardens of all fungus-growing ants examined, we found taxonomically unique and diverse microbial yeast communities across the different fungicultures. Ascomycete yeasts were the core taxa in fungus garden samples, with Saccharomycetales as the most frequent order. The genera Aureobasidium, Candida, Papiliotrema, Starmerella, and Sugiyamaella had the highest incidence in fungus gardens. Despite the expected similarity within the same fungiculture system, colonies of the same ant species differed in community structure. Among Saccharomycotina yeasts, few were distinguishable as killer yeasts, with a classical inhibition pattern for the killer phenotype, differing from earlier observations in this environment, which should be further investigated. Yeast mycobiome in fungus gardens is distinct between colonies of the same fungiculture and each ant colony harbors a distinguished and unique yeast community. Fungus gardens of attine ants are emergent environments to study the diversity and ecology of yeasts associated with insects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Data supporting the results in the paper are available in the Supplementary Material.

References

  1. Buzzini P, Lachance MA, Yurkov A (2017) Yeasts in natural ecosystems: diversity. Basel, Switzerland: Springer International Publishing 499.https://doi.org/10.1007/978-3-319-62683-3

  2. Brysch-Herzberg M (2004) Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50(2):87–100

    CAS  PubMed  Google Scholar 

  3. da Costa Neto DJ, de Morais PB (2020) The vectoring of Starmerella species and other yeasts by stingless bees in a Neotropical savanna. Fungal Ecol 47:100973

    Google Scholar 

  4. Ganter PF (1988) The vectoring of cactophilic yeasts by Drosophila. Oecologia 75(3):400–404

    PubMed  Google Scholar 

  5. Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1(1):1–8

    CAS  PubMed  Google Scholar 

  6. Stefanini I (2018) Yeast-insect associations: it takes guts. Yeast 35(4):315–330

    CAS  PubMed  Google Scholar 

  7. Reuter M, Bell G, Greig D (2007) Increased outbreeding in yeast in response to dispersal by an insect vector. Curr Biol 17(3):R81–R83

    CAS  PubMed  Google Scholar 

  8. Stefanini I, Dapporto L, Berná L, Polsinelli M, Turillazzi S, Cavalieri D (2016) Social wasps are a Saccharomyces mating nest. Proc Natl Acad Sci 113(8):2247–2251

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Seike T, Sakata N, Matsuda F, Furusawa C (2021) Elevated sporulation efficiency in fission yeast Schizosaccharomyces japonicus strains isolated from Drosophila. J Fungi 7(5):350

    CAS  Google Scholar 

  10. Möller A (1893) Die Pilzgärten einiger südamerikanischer Ameisen (No. 6). G. Fischer.

  11. Weber NA (1972) The fungus-culturing behavior of ants. Am Zool 12(3):577–587

    Google Scholar 

  12. Branstetter MG, Ješovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC, Brady SG, Schultz TR (2017) Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc Royal Soc B: Biol Sci 284(1852):20170095

    Google Scholar 

  13. Nygaard S et al (2016) Reciprocal genomic evolution in the ant–fungus agricultural symbiosis. Nat Commun 7(1):1–9

    Google Scholar 

  14. Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci 105(14):5435–5440

    CAS  PubMed  PubMed Central  Google Scholar 

  15. de Angelis C, Serzedello A, De Angelis DF (1983) Yeasts found in gardens of Atta sexdens rubropilosa and Atta laevigata. Naturalia 8:149–151

    Google Scholar 

  16. Carreiro SC, Pagnocca FC, Bueno OC, Júnior MB, Hebling MJA, da Silva OA (1997) Yeasts associated with nests of the leaf-cutting ant Atta sexdens rubropilosa Forel, 1908. Antonie Van Leeuwenhoek 71(3):243–248

    CAS  PubMed  Google Scholar 

  17. Craven SE, Dix MW, Michaels GE (1970) Attine fungus gardens contain yeasts. Science 169(3941):184–186

    CAS  PubMed  Google Scholar 

  18. Fisher PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leaf-cutting ant Atta cephalotes: a preliminary study. Mycol Res 100(5):541–546

    Google Scholar 

  19. Pagnocca FC, Carreiro SC, Bueno OC, Hebling MJ, Da Silva OA (1996) Microbiological changes in the nests of leaf-cutting ants fed on sesame leaves. J Appl Entomol 120(1–5):317–320

    Google Scholar 

  20. Bizarria Jr R, Pagnocca FC, Rodrigues A (2021) Yeasts in the attine ant–fungus mutualism: diversity, functional roles, and putative biotechnological applications. Yeast.

  21. Schultz TR, Sosa-Calvo J, Brady SG, Lopes CT, Mueller UG, Bacci M Jr, Vasconcelos HL (2015) The most relictual fungus-farming ant species cultivates the most recently evolved and highly domesticated fungal symbiont species. Am Nat 185(5):693–703

    PubMed  Google Scholar 

  22. Cristiano MP, Cardoso DC, Sandoval‐Gómez VE, Simões‐Gomes FC (2020) Amoimyrmex Cristiano, Cardoso and Sandoval, gen. nov. (Hymenoptera: Formicidae): a new genus of leaf‐cutting ants revealed by multilocus molecular phylogenetic and morphological analyses. Austral Entomol 59(4):643–676.

  23. de Fine Licht HH, Boomsma JJ (2010) Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecol Entomol 35(3):259–269

    Google Scholar 

  24. Ronque MUV, Feitosa RM, Oliveira PS (2019) Natural history and ecology of fungus-farming ants: a field study in Atlantic rainforest. Insectes Soc 66(3):375–387

    Google Scholar 

  25. Arcuri SL, Pagnocca FC, da Paixão Melo WG, Nagamoto NS, Komura DL, Rodrigues A (2014) Yeasts found on an ephemeral reproductive caste of the leaf-cutting ant Atta sexdens rubropilosa. Antonie Van Leeuwenhoek 106(3):475–487

    PubMed  Google Scholar 

  26. Rodrigues A, Cable RN, Mueller UG, Bacci M, Pagnocca FC (2009) Antagonistic interactions between garden yeasts and microfungal garden pathogens of leaf-cutting ants. Antonie Van Leeuwenhoek 96(3):331–342

    PubMed  Google Scholar 

  27. Pagnocca FC, Rodrigues A, Nagamoto NS, Bacci M (2008) Yeasts and filamentous fungi carried by the gynes of leaf-cutting ants. Antonie Van Leeuwenhoek 94(4):517–526

    PubMed  Google Scholar 

  28. Sampaio JP, Gadanho M, Santos S, Duarte FL, Pais C, Fonseca A, Fell JW (2001) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51(2):687–697

    CAS  PubMed  Google Scholar 

  29. Meyer W, Mitchell TG, Freedman EZ, Vilgalys R (1993) Hybridization probes for conventional DNA fingerprinting used as single primers in the polymerase chain reaction to distinguish strains of Cryptococcus neoformans. J Clin Microbiol 31(9):2274–2280

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73(4):331–371

    CAS  PubMed  Google Scholar 

  31. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symp Ser 41:95–98.

  32. Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166

    CAS  PubMed  Google Scholar 

  33. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274

    CAS  PubMed  Google Scholar 

  34. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35(21):4453–4455

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard SA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542

    PubMed  PubMed Central  Google Scholar 

  36. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proc Gateway Comput Environ Work (GCE), 14 Nov. 2010, New Orleans, LA pp 1–8.

  37. Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rambaut A (2016) Figtree v. 1.4.3. http://tree.bio.ed.ac.uk/software/figtree/2016.

  39. Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11(1):1–9

    Google Scholar 

  40. Crabtree AM, Kizer EA, Hunter SS, Van Leuven JT, New DD, Fagnan MW, Rowley PA (2019) A rapid method for sequencing double-stranded RNAs purified from yeasts and the identification of a potent K1 killer toxin isolated from Saccharomyces cerevisiae. Viruses 11(1):70

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi (Kenya). http://www.worldagroforestry.org/output/tree-diversity-analysis.

  42. Oksanen JF et al (2020) Vegan: community ecology package. R Package Version 2:5–7. https://CRAN.R-project.org/package=vegan.

  43. Chao A, Gotelli NJ, Hsieh TC, Sande EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67

    Google Scholar 

  44. Hsieh TC, Ma KH Chao A (2020) iNEXT: interpolation and extrapolation for species diversity. R package version 2.0.20, http://chao.stat.nthu.edu.tw/wordpress/software_download/.

  45. R Core Team (2021) R: a language and environment for statistical computing.; R Foundation for Statistical Computing: Vienna, Austria, 2021; Available online: https://www.R-project.org/ (accessed on 20 December 2021).

  46. Dusa A. (2021) Venn: draw Venn diagrams. R package version 1.10. https://CRAN.R-project.org/package=venn

  47. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129(2):271–280

    PubMed  Google Scholar 

  48. Roberts DW (2019) Labdsv: ordination and multivariate analysis for ecology. R package version 2.0–1. https://CRAN.R-project.org/package=labdsv.

  49. RStudio Team (2021) RStudio: integrated development environment for R.; RStudio, PBC: Boston, MA, USA, 2021; Available online: http://www.rstudio.com/ (accessed on 20 December 2021).

  50. Melo WGP, de Oliveira TB, Arcuri SL, de Morais PB, Pagnocca FC (2021) Yeasts in the nests of the leaf-cutter ant Acromyrmex balzani in a Savanna biome: exploitation of community and metabolic diversity. Antonie Van Leeuwenhoek 114(6):751–764

    CAS  PubMed  Google Scholar 

  51. Blanton CM, Ewel JJ (1985) Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology 66(3):861–869

    Google Scholar 

  52. Mueller UG, Rabeling C (2008) A breakthrough innovation in animal evolution. Proc Natl Acad Sci USA 105(14):5287–5288

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Nguyen NH, Suh SO, Blackwell M (2007) Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99(6):842–858

    CAS  PubMed  Google Scholar 

  54. Suh SO, McHugh JV, Pollock DD, Backwell M (2005) The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109(3):261–265

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Suh SO, Nguyen NH, Blackwell M (2008) Yeasts isolated from plant-associated beetles and other insects: seven novel Candida species near Candida albicans. FEMS Yeast Res 8(1):88–102

    CAS  PubMed  Google Scholar 

  56. Urbina H, Schuster J, Blackwell M (2013) The gut of Guatemalan passalid beetles: a habitat colonized by cellobiose-and xylose-fermenting yeasts. Fungal Ecol 6(5):339–355.

  57. Rodrigues A, Mueller UG, Ishak HD, Bacci M Jr, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78(2):244–255

    CAS  PubMed  Google Scholar 

  58. Leal-Dutra CA, Griffith GW, Neves MA, McLaughlin DJ, McLaughlin EG, Clasen LA, Dentinger B (2020) Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) introducing the ant-associated genus Myrmecopterula gen. nov., Phaeopterula Henn. and the corticioid Radulomycetaceae fam. nov. IMA Fungus 11(1):1–24.

  59. Lachance MA, Rosa CA, Starmer WT, Schlag-Edler BIRGIT, Barker JSF, Bowles JM (1998) Wickerhamiella australiensis, Wickerhamiella cacticola, Wickerhamiella occidentalis, Candida drosophilae and Candida lipophila, five new related yeast species from flowers and associated insects. Int J Syst Evol Microbiol 48(4):1431–1443

    Google Scholar 

  60. Sena LM, Morais CG, Lopes MR, Santos RO, Uetanabaro A, Morais PB, Vital MJS, Morais MA Jr, Lachance MA, Rosa CA (2017) d-Xylose fermentation, xylitol production and xylanase activities by seven new species of Sugiyamaella. Antonie Van Leeuwenhoek 110(1):53–67

    CAS  PubMed  Google Scholar 

  61. Shi CF, Zhang KH, Chai CY, Yan ZL, Hui FL (2021) Diversity of the genus Sugiyamaella and description of two new species from rotting wood in China. MycoKeys 77:27

    PubMed  PubMed Central  Google Scholar 

  62. Kurtzman CP (2011) Yamadazyma Billon-Grand (1989). The yeasts: a taxonomic study. Elsevier Science, Amsterdam, pp 919–925

    Google Scholar 

  63. Yurkov AM (2018) Yeasts of the soil–obscure but precious. Yeast 35(5):369–378

    CAS  PubMed  Google Scholar 

  64. Lee YM, Lee H, Heo YM, Hong JH, Jang S, Kang KY, Kim JJ (2017) Phylogenetic analysis of wood-inhabiting molds and assessment of soft-rot wood deterioration. Part 5. Genus Aureobasidium. Holzforschung 71(5):437–443

    CAS  Google Scholar 

  65. Isaeva OV, Glushakova AM, Yurkov AM, Chernov IY (2009) The yeast Candida railenensis in the fruits of English oak (Quercus robur L.). Microbiology 78(3):355–359

    CAS  Google Scholar 

  66. Maksimova IA, Glushakova AM, Kachalkin AV, Chernov IY, Panteleeva SN, Reznikova ZI (2016) Yeast communities of Formica aquilonia colonies. Microbiology 85(1):124–129

    CAS  Google Scholar 

  67. Santos ARDO, Lee DK, Ferreira AG, do Carmo MC, Rondelli VM, Barros KO, Hsiang T, Rosa CA, Lachance MA (2020) The yeast community of Conotelus sp. (Coleoptera: Nitidulidae) in Brazilian passionfruit flowers (Passiflora edulis) and description of Metschnikowia amazonensis sp. nov., a large‐spored clade yeast. Yeast 37(3):253–260

    CAS  PubMed  Google Scholar 

  68. Arrey G, Li G, Murphy R, Guimaraes L, Alizadeh S, Poulsen M, Regenberg B (2021) Isolation, characterization, and genome assembly of Barnettozyma botsteinii sp. nov. and novel strains of Kurtzmaniella quercitrusa isolated from the intestinal tract of the termite Macrotermes bellicosus. G3 11(12):jkab342.

  69. Somers JM, Bevan EA (1969) The inheritance of the killer character in yeast. Genet Res 13(1):71–83

    CAS  PubMed  Google Scholar 

  70. Woods DR, Bevan EA (1968) Studies on the nature of the killer factor produced by Saccharomyces cerevisiae. Microbiology 51(1):115–126

    CAS  Google Scholar 

  71. Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997) Yeast killer systems. Clin Microbiol Rev 10(3):369–400

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Marquina D, Santos A, Peinado J (2002) Biology of killer yeasts. Int Microbiol 5(2):65–71

    CAS  PubMed  Google Scholar 

  73. Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4(3):212–221

    CAS  PubMed  Google Scholar 

  74. Schmitt M, Brendel M, Schwarz R, Radler F (1989) Inhibition of DNA synthesis in Saccharomyces cerevisiae by yeast killer toxin KT28. Microbiology 135(6):1529–1535

    CAS  Google Scholar 

  75. Schmitt MJ, Reiter J (2008) Viral induced yeast apoptosis. Biochimica et Biophysica Acta (BBA)-Mol Cell Res 1783(7):1413–1417.

  76. Schmitt MJ, Klavehn P, Wang J, Schönig I, Tipper DJ (1996) Cell cycle studies on the mode of action of yeast K28 killer toxin. Microbiology 142(9):2655–2662

    CAS  PubMed  Google Scholar 

  77. Carreiro SC, Pagnocca FC, Bacci M, Bueno OC, Hebling MJA, Middelhoven WJ (2002) Occurrence of killer yeasts in leaf-cutting ant nests. Folia Microbiol 47(3):259–262

    CAS  Google Scholar 

  78. Robledo-Leal E, Elisondo-Zatuche M, Treviño-Rangel RJ, González GM, Hernández-Luna C (2016) Isolation of killer yeasts from ants of the genus Atta and their effect on the red tomato’s fungal pathogen Geotrichum candidum. Mex J Phytopathol 34:258–269

    Google Scholar 

  79. Sipiczki M (2020) Metschnikowia pulcherrima and related pulcherrimin-producing yeasts: fuzzy species boundaries and complex antimicrobial antagonism. Microorganisms 8(7):1029

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Boynton PJ (2019) The ecology of killer yeasts: interference competition in natural habitats. Yeast 36(8):473–485

    CAS  PubMed  Google Scholar 

  81. Case TJ, Gilpin ME (1974) Interference competition and niche theory. Proc Natl Acad Sci 71(8):3073–3077

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Philliskirk G, Young TW (1975) The occurrence of killer character in yeasts of various genera. Antonie Van Leeuwenhoek 41(1):147–151

    CAS  PubMed  Google Scholar 

  83. Pieczynska MD, de Visser JAG, Korona R (2013) Incidence of symbiotic dsRNA ‘killer’ viruses in wild and domesticated yeast. FEMS Yeast Res 13(8):856–859

    CAS  PubMed  Google Scholar 

  84. Chang SL, Leu JY, Chang TH (2015) A population study of killer viruses reveals different evolutionary histories of two closely related Saccharomyces sensu stricto yeasts. Mol Ecol 24(16):4312–4322

    CAS  PubMed  Google Scholar 

  85. Carreiro SC (2000) Pesquisa de fator killer e análise da degradação de polissacarídeos vegetais por leveduras associadas aos ninhos de Atta sexdens. PhD thesis, UNESP, Rio Claro, São Paulo, Brazil.

  86. Mendes TD, Rodrigues A, Dayo-Owoyemi I, Marson FA, Pagnocca FC (2012) Generation of nutrients and detoxification: possible roles of yeasts in leaf-cutting ant nests. Insects 3(1):228–245

    PubMed  PubMed Central  Google Scholar 

  87. Silva A, Bacci M Jr, de Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJA (2003) Survival of Atta sexdens workers on different food sources. J Insect Physiol 49(4):307–313

    CAS  PubMed  Google Scholar 

  88. Cappelli A, Ulissi U, Valzano M, Damiani C, Epis S, Gabrielli MG, Conti S, Polonelli L, Bandi C, Favia G, Ricci I (2014) A Wickerhamomyces anomalus killer strain in the malaria vector Anopheles stephensi. PLoS ONE 9(5):e95988

    PubMed  PubMed Central  Google Scholar 

  89. Cappelli A, Valzano M, Cecarini V, Bozic J, Rossi P, Mensah P, Amantini C, Favia G, Ricci I (2019) Killer yeasts exert anti-plasmodial activities against the malaria parasite Plasmodium berghei in the vector mosquito Anopheles stephensi and in mice. Parasit Vectors 12(1):1–8

    CAS  Google Scholar 

  90. Perez MF, Contreras L, Garnica NM, Fernández-Zenoff MV, Farías ME, Sepulveda M, Ramallo J, Dib JR (2016) Native killer yeasts as biocontrol agents of postharvest fungal diseases in lemons. PLoS ONE 11(10):e0165590

    PubMed  PubMed Central  Google Scholar 

  91. Polonelli L, Morace G (1986) Reevaluation of the yeast killer phenomenon. J Clin Microbiol 24(5):866–869

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Laura de Carvalho Pereira Vieira, Nilson Satoru Nagamoto, and Pepijn W. Kooij for fieldwork support, and Renata de Oliveira Aquino Zani for sequencing assistance. We also thank Juliana Aparecida dos Santos for insights into a previous version of this manuscript. Samples collected in Rio Claro, SP, Brazil, were conducted under the ICMBio collecting permit #31534-4 issued to AR. The study also follows the Nagoya Protocol, under the SISGEn permit # A877F11 issued to AR.

Funding

The study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (grant #2019/03746–0 and #2019/24412–2). The study was also supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Financial Code 001 with a scholarship to TCP. AR and RBJ also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a research fellowship and a scholarship (grant #305269/2018–6 and #142396/2019–2, respectively).

Author information

Authors and Affiliations

  1. Department of General and Applied Biology, São Paulo State University (UNESP), Bela Vista, Avenida 24-A, n. 1515SP 13.506-900, Rio Claro, Brazil

    Rodolfo Bizarria Jr., Tatiane de Castro Pietrobon & Andre Rodrigues

  2. Center for the Study of Social Insects, São Paulo State University (UNESP), Rio Claro, SP, Brazil

    Rodolfo Bizarria Jr., Tatiane de Castro Pietrobon & Andre Rodrigues

Authors
  1. Rodolfo Bizarria Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatiane de Castro Pietrobon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andre Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RB and AR designed the study. All authors participated in the field expeditions. RB and TCP engaged in laboratory work. RB analyzed the data. RB and AR wrote the manuscript.

Corresponding author

Correspondence to Andre Rodrigues.

Ethics declarations

Ethics Approval

No ethical approval was needed for this work.

Competing Interests

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 5.39 MB)

Supplementary file2 (DOCX 59.3 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bizarria, R., de Castro Pietrobon, T. & Rodrigues, A. Uncovering the Yeast Communities in Fungus-Growing Ant Colonies. Microb Ecol 86, 624–635 (2023). https://doi.org/10.1007/s00248-022-02099-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-022-02099-1

Keywords

Search

Navigation