The digestive tract of Phylloicus (Trichoptera: Calamoceratidae) harbours different yeast taxa in Cerrado streams, Brazil

Abstract

The interaction between insects, both larval and adult, and yeasts associated with their digestive tract (DT), has been of interest in recent years, since it can be beneficial for both partners. Studies focusing on this habitat have contributed to the expansion of knowledge about diversity, biogeography and functional characterization of yeasts, especially in ecosystems still poorly exploited, such as the Brazilian Cerrado. We investigated the interaction between larvae of Phylloicus spp. (Trichoptera: Calamoceratidae), which is an aquatic insect, and the yeasts isolated from its DT. The larvae were collected from first-order Cerrado streams of two States (Mato Grosso – MT and Pará – PA) in Brazil. Yeasts were cultivated and identified based on sequence analysis of the D1/D2 domains of the large subunit of rRNA genes. A total of 20 yeast species, belonging to six genera of Ascomycota and five Basidiomycota, is harbored in the DT of the larvae. The most frequent genera were Candida, Papiliotrema, Rhodotorula (19.3% each) and Issatchenkia (15.8%). Candida parapsilosis and Rhodotorula mucilaginosa were only yeast species isolated from the DT of larvae in both locations. The most species-rich community was that associated with DT of Phylloicus spp. in MT samples (H′ = 1.48) as compared to PA samples (H′ = 0.67). All species were accidental (frequency < 25%), which is indicative of a loose association of these yeasts with their host. This is the first report of the association of yeasts with the DT of the shredders group of aquatic insects.

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References

  1. Afonso AAO, Henry R, Rodella RCSM (2000) Allochthonous matter input in two different stretches of a headstream (Itatinga, São Paulo, Brazil). Braz Arch Biol Technol 43(3):335–343. https://doi.org/10.1590/S1516-89132000000300014

    Article  Google Scholar 

  2. Altschul SF, Gish W, Miller W, Myers EW (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    CAS  Article  Google Scholar 

  3. Araújo FV, Soares CAG, Hagler AN, Mendonça-Hagler LC (1995) Ascomycetous yeast communities of marine invertebrates in a Southeast Brazilian mangrove ecosystem. Antonie Van Leeuwenhoek 68(2):91–99. https://doi.org/10.1007/BF00873096

    Article  PubMed  Google Scholar 

  4. Araújo FV, Rosa CA, Freitas LFD, Lachance MA, Vaughan-Martini A, Mendonca-Hagler LC, Hagler AN (2012) Kazachstania bromeliacearum sp. nov., a yeast species from water tanks of bromeliads. Int J Syst Evol Microbiol 62(4):1002–1006. https://doi.org/10.1099/ijs.0.031633-0

    Article  PubMed  Google Scholar 

  5. Asahina S (1964) Food material and feeding procedures for mosquito larvae. Bull World Health Organ 31:465–466

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Ba AS, Phillips SA Jr (1996) Yeast biota of the red imported fire ant. Mycol Res 100(6):740–746. https://doi.org/10.1016/S0953-7562(96)80208-5

    Article  Google Scholar 

  7. Bambi P, Souza Rezende R, Feio MJ, Leite GFM, Alvin E, Quintão JMB, Araújo F, Gonçalves Júnior JF (2016) Temporal and spatial patterns in inputs and stock of organic matter in savannah streams of Central Brazil. Ecosystems 20(4):757–768. https://doi.org/10.1007/s10021-016-0058-z

    Article  Google Scholar 

  8. Brandão LR, Vaz ABM, Santo LCE, Pimenta RS, Morais PB, Libkind D, Rosa LH, Rosa CA (2017) Diversity and biogeographical patterns of yeast communities in Antarctic, Patagonian and tropical lakes. Fungal Ecol 28:33–43. https://doi.org/10.1016/j.funeco.2017.04.003

    Article  Google Scholar 

  9. Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3(4):307–321. https://doi.org/10.4161/gmic.19896

    Article  PubMed  PubMed Central  Google Scholar 

  10. Buzzini P, Martini A (2002) Extracellular enzymatic activity profiles in yeast and yeast like strains isolated from tropical environments. J Appl Microbiol 93(6):1020–1025

    CAS  Article  Google Scholar 

  11. Canhoto C, Graça MAS, Barlöcher F (2005) Feeding preferences. In: Graça M, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition – a practical guide. Springer, Dordrecht

    Google Scholar 

  12. Chang C, Lee C, Lin K, Liu S (2016) Diversity of yeasts associated with the sea surface microlayer and underlying water along the northern coast of Taiwan Diversity of yeasts associated with the sea surface microlayer and underlying water along the northern coast of Taiwan. Res Microbiol 167:35–45. https://doi.org/10.1016/j.resmic.2015.08.005

    Article  PubMed  Google Scholar 

  13. Chen HW, Chou JY, Lin CC, Wen Y-D, Wang WL (2016) Seasonal yeast compositions in Forcipomyia taiwana (Diptera: Ceratopogonidae). J Asia Pac Entomol 19(2):509–514. https://doi.org/10.1016/j.aspen.2016.04.020

    Article  Google Scholar 

  14. Chi ZM, Liu TT, Chi Z, Liu GL, Wang ZP (2012) Occurrence and diversity of yeasts in the mangrove ecosystems in Fujian, Guangdong and Hainan provinces of China. Indian J Microbiol 52(3):346–353. https://doi.org/10.1007/s12088-012-0251-5

    Article  PubMed  PubMed Central  Google Scholar 

  15. Christiaens JF, Franco LM, Cools TL, Meester LD, Michiels J, Wenseleers T (2014) The fungal aroma gene ATF1 promotes dispersal of yeast cells through insect vectors. Cell Rep 9(2):425–432. https://doi.org/10.1016/j.celrep.2014.09.009

    CAS  Article  PubMed  Google Scholar 

  16. Coelho MA, Almeida JMF, Martins IM, Silva AJ, Sampaio JP (2010) The dynamics of the yeast community of the Tagus river estuary: testing the hypothesis of the multiple origins of estuarine yeasts. Anton Leeuw 98(3):331–342. https://doi.org/10.1007/s10482-010-9445-1

    Article  Google Scholar 

  17. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. https://doi.org/10.1146/annurev-ento-010814-020822

    CAS  Article  PubMed  Google Scholar 

  18. Ferreira WR, Ligeiro R, Macedo DR, Hughes RM, Kaufmann PR, Oliveira LG, Callisto M (2015) Is the diet of a typical shredder related to the physical habitat of headwater streams in the Brazilian Cerrado? Ann Limnol Int J Limnol 51(2):115–127. https://doi.org/10.1051/limn/2015004

    Article  Google Scholar 

  19. França JS, Gregorio RS, Paula JDA, Gonçalves Junior JF, Ferreira FA, Callisto M (2009) Composition and dynamics of allochthonous organic matter inputs and benthic stock in a Brazilian stream. Mar Freshw Res 60(10):990–998. https://doi.org/10.1071/MF08247

    Article  Google Scholar 

  20. Gan HM, Thomas BN, Cavanaugh NT, Morales GH, Mayers AN, Savka MA, Hudson AO (2017) Whole genome sequencing of Rhodotorula mucilaginosa isolated from the chewing stick (Distemonanthus benthamianus): insights into Rhodotorula phylogeny, mitogenome dynamics and carotenoid biosynthesis. PerrJ 5:1–18. https://doi.org/10.7717/peerj.4030

    CAS  Article  Google Scholar 

  21. Geib SM, Jimenez-Gasco MDM, Carlson JE, Tien M, Hoover K (2009) Effect of host tree species on cellulase activity and bacterial community composition in the gut of larval asian longhorned beetle. Environ Entomol 38(3):686–699. https://doi.org/10.1603/022.038.0320

    CAS  Article  PubMed  Google Scholar 

  22. Gimenes KZ, Cunha-Santino MB, Bianchini I Jr (2010) Decomposição De Matéria Orgânica Alóctone E Autóctone Em Ecossistemas Aquáticos. Oecologia 14(04):1036–1073. https://doi.org/10.4257/oeco.2010.1404.13

    Article  Google Scholar 

  23. Gomes PP, Medeiros AO, Gonçalves Júnior JF (2016) The replacement of native plants by exotic species may affect the colonization and reproduction of aquatic hyphomycetes. Limnologica 59:124–130. https://doi.org/10.1016/j.limno.2016.05.005

    CAS  Article  Google Scholar 

  24. Gonçalves JF Jr, Callisto M (2013) Organic-matter dynamics in the riparian zone of a tropical headwater stream in Southern Brasil. Aquat Bot 109:8–13. https://doi.org/10.1016/j.aquabot.2013.03.005

    Article  Google Scholar 

  25. Gonçalves AL, Chauvet E, Bärlocher F, Graça MAS, Canhoto C (2014) Top-down and bottom-up control of litter decomposers in streams. Freshw Biol 59(10):2172–2182. https://doi.org/10.1111/fwb.12420

    Article  Google Scholar 

  26. Gonçalves AL, Lírio AV, Graça MAS, Canhoto C (2016) Fungal species diversity affects leaf decomposition after drought. Int Rev Hydrobiol 101(1–2):78–86. https://doi.org/10.1002/iroh.201501817

    Article  Google Scholar 

  27. Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams – a review. Int Rev Hydrobiol 86(4–5):383–393. https://doi.org/10.1002/1522-2632

    Article  Google Scholar 

  28. Graça M, Cressa C, Gessner M, Feio M, Callies K, Barrios C (2001) Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshw Biol 46(7):947–957. https://doi.org/10.1046/j.1365-2427.2001.00729.x

    Article  Google Scholar 

  29. Graça MAS, Cressa C (2010) Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int Rev Hydrobiol 95(1):27–41. https://doi.org/10.1002/iroh.200911173

    Article  Google Scholar 

  30. Graça MAS, Maltby L, Calow P (1993a) Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I: feeding strategies. Oecologia 93:139–144

    Article  Google Scholar 

  31. Graça MAS, Maltby L, Calow P (1993b) Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus II: effects on growth, reproduction and physiology. Oecologia 96:304–309

    Article  Google Scholar 

  32. Grünwald S, Pilhofer M, Höll W (2010) Microbial associations in gut systems of wood- and bark-inhabiting longhorned beetles [Coleoptera: Cerambycidae]. Syst Appl Microbiol 33(1):25–34. https://doi.org/10.1016/j.syapm.2009.10.002

    CAS  Article  PubMed  Google Scholar 

  33. Gujjari P, Suh S-O, Lee C-F, Zhou JJ (2011) Trichosporon xylopini sp. nov., a hemicellulose-degrading yeast isolated from the wood-inhabiting beetle Xylopinus saperdioides. Int J Syst Evol Microbiol 61(10):2538–2542. https://doi.org/10.1099/ijs.0.028860-0

    Article  PubMed  Google Scholar 

  34. Gusmão DS, Santos AV, Marini DC, Bacci M, Berbert-Molina MA, Lemos FJA (2010) Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop 115(3):275–281. https://doi.org/10.1016/j.actatropica.2010.04.011

    Article  PubMed  Google Scholar 

  35. Hamada N, Ferreira-Keppler RL (Org.) (2012) Guia ilustrado de insetos aquáticos e semiaquáticos da Reserva Florestal Ducke. Manaus: EDUA, 198p

  36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  37. Han SM, Hyun SH, Lee HB, Lee HW, Kim HK, Lee JS (2015) Isolation and identification of yeasts from wild flowers collected around Jangseong Lake in Jeollanam-do, Republic of Korea, and characterization of the unrecorded yeast Bullera coprosmaensis. Mycobiology 43(3):266–271. https://doi.org/10.5941/MYCO.2015.43.3.266

    Article  PubMed  PubMed Central  Google Scholar 

  38. Handel S, Wang T, Yurkov AM, König H (2016) Sugiyamaella mastotermitis sp. nov. and Papiliotrema odontotermitis f.a., sp. nov. from the gut of the termites Mastotermes darwiniensis and Odontotermes obesus. Int J Syst Evol Microbiol 66(11):4600–4608. https://doi.org/10.1099/ijsem.0.001397

    CAS  Article  PubMed  Google Scholar 

  39. Hieber M, Gessner MO (2002) Contribution of stream detritivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83(4):1026–1038. https://doi.org/10.1890/0012-9658

    Article  Google Scholar 

  40. Hongoh Y, Ishikawa H (2000) Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. J Mol Evol 51(3):265–277. https://doi.org/10.1007/s002390010088

    CAS  Article  PubMed  Google Scholar 

  41. Hu K, Zhu XL, Mu H, Ma Y, Ullah N, Tao YS (2016) A novel extracellular glycosidase activity from Rhodotorula mucilaginosa: its application potential in wine aroma enhancement. Lett Appl Microbiol 62(2):169–176. https://doi.org/10.1111/lam.12527

    CAS  Article  PubMed  Google Scholar 

  42. Jaiboon K, Lertwattanasakul N, Limtong P, Limtong S (2016) Yeasts from peat in a tropical peat swamp forest in Thailand and their ability to produce ethanol, indole-3-acetic acid and extracellular enzymes. Mycol Prog 15(7):755–770. https://doi.org/10.1007/s11557-016-1205-9

    Article  Google Scholar 

  43. Jiménez M, González AE, Martínez MJ, Martínez AT, Dale BE (1991) Screening of yeasts isolated from decayed wood for lignocellulose-degrading enzyme activities. Mycol Res 95(11):1299–1302. https://doi.org/10.1016/S0953-7562(09)80578-9

    Article  Google Scholar 

  44. Kanti A, Sudiana M (2002) Cellulolytic yeast isolated from soil Gunung Halimun National Park. B’erita Biologi 6:85–90

    Google Scholar 

  45. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  46. Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19(3):707–713. https://doi.org/10.1111/j.1523-1739.2005.00702.x

    Article  Google Scholar 

  47. Krauss GJ, Solé M, Krauss G, Schlosser D, Wesenberg D, Bärlocher F (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol Rev 35(4):620–651. https://doi.org/10.1111/j.1574-6976.2011.00266.x

    CAS  Article  PubMed  Google Scholar 

  48. Krebs CJ (1978) Ecology: The experimental analysis of distribution and abundance, 2nd edn. Harper & Row, New York

    Google Scholar 

  49. Kuo H, Zeng J-K, Wang P-H, Chen W-C (2015) A novel exo-glucanase explored from a Meyerozyma sp. fungal strain. Adv. Enzyme Res 3:53–65

    CAS  Article  Google Scholar 

  50. Kurtzman CP, Fell JW, Boekhout T, Robert V (2011a) Methods for the isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, fifth edn. Elsevier, Amsterdam, pp 87–110

  51. Kurtzman CP, Fell JW, Boekhout T (2011b) Gene sequence analyses and other DNA-based methods for yeast species recognition. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, fifth edn. Elsevier, Amsterdam, pp 137–144

    Google Scholar 

  52. Lachance MA, Bowles JM, Starmer WT, Barker JSF (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 45(2):172–177. https://doi.org/10.1139/w98-225

    CAS  Article  PubMed  Google Scholar 

  53. Lachance MA, Bowles JM, Chavarria-Diaz MM, Janzen DH (2001) Candida cleridarum, Candida tilneyi, and Candida powellii, three new yeast species isolated from insects associated with flowers. Int J Syst Evol Microbiol 51(3):1201–1207. https://doi.org/10.1099/00207713-51-3-1201

    CAS  Article  PubMed  Google Scholar 

  54. Lachance M-A, Boekhout T, Scorzetti G, Fell JW, Kurtzman CP (2011) Candida Berkhout (1923). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, fifth edn. Elsevier, Amsterdam, pp 987–1278

    Google Scholar 

  55. León AV-P, Sanchez-Flores A, Rosenblueth M, Martínez-Romero E (2016) Fungal community associated with Dactylopius (Hemiptera: Coccoidea: Dactylopiidae) and its role in uric acid metabolism. Front Microbiol 7:1–15. https://doi.org/10.3389/fmicb.2016.00954

    Article  Google Scholar 

  56. Li M, Liu GL, Chi Z, Chi ZM (2010) Single cell oil production from hydrolysate of cassava starch by marine-derived yeast Rhodotorula mucilaginosa TJY15a. Biomass Bioenergy 34(1):101–107. https://doi.org/10.1016/j.biombioe.2009.10.005

    CAS  Article  Google Scholar 

  57. Limtong S, Kaewwichian R, Yongmanitchai W, Kawasaki H (2014) Diversity of culturable yeasts in phylloplane of sugarcane in Thailand and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 30(6):1785–1796. https://doi.org/10.1007/s11274-014-1602-7

    CAS  Article  PubMed  Google Scholar 

  58. Liu XZ, Wang Q-M, Göker M, Groenewald M, Kachalkin AV, Lumbsch HT, Millanes AM, Wedin M, Yurkov AM, Boekhout T, Bai F-Y (2015a) Towards an integrated phylogenetic classification of the Tremellomycetes. Stud Mycol 81:85–147. https://doi.org/10.1016/j.simyco.2015.12.001

    Article  PubMed  Google Scholar 

  59. Liu X-Z, Wang Q-M, Theelen B, Groenewald M, Bai FY, Boekhout T (2015b) Phylogeny of tremellomycetous yeasts and related dimorphic and filamentous basidiomycetes reconstructed from multiple gene sequence analyses. Stud Mycol 81:1–26. https://doi.org/10.1016/j.simyco.2015.08.001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. Lou QZ, Lu M, Sun JH (2014) Yeast diversity associated with invasive Dendroctonus valens killing Pinus tabuliformis in China using culturing and molecular methods. Microbiol Ecol 68(2):397–415. https://doi.org/10.1007/s00248-014-0413-6

    Article  Google Scholar 

  61. Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer on methods and computing. John Wiley, New York

    Google Scholar 

  62. Maijala P, Fagerstedt KV, Raudaskoski M (1991) Detection of extracellular cellulolytic and proteolytic activity in ectomycorrhizal fungi and Heterobasidion annosum (Fr.). New Phytol 117:643–648

    CAS  Article  Google Scholar 

  63. Martins GM, Bocchini-Martins DA, Bezzerra-Bussoli C, Pagnocca FC, Boscolo M, Monteiro DA, Silva R, Gomes E (2018) The isolation of pentose-assimilating yeasts and their xylose fermentation potential. Braz J Microbiol 49(1):162–168. https://doi.org/10.1016/j.bjm.2016.11.014

    CAS  Article  PubMed  Google Scholar 

  64. Mathew GM, Ju YM, Lai CY, Mathew DC, Huang CC (2012) Microbial community analysis in the termite gut and fungus comb of Odontotermes formosanus: the implication of Bacillus as mutualists. FEMS Microbiol Ecol 79(2):504–517. https://doi.org/10.1111/j.1574-6941.2011.01232.x

    CAS  Article  PubMed  Google Scholar 

  65. McCune B, Grace JB (2002) Analysis of ecological communities. MjM software design, Gleneden Beach, Oregon

  66. Medeiros AO, Kohler LM, Hamdan JS, Missagia BS, Barbosa FAR, Rosa CA (2008) Diversity and antifungal susceptibility of yeasts from tropical freshwater environments in southeastern Brazil. Water Res 42(14):3921–3929. https://doi.org/10.1016/j.watres.2008.05.026

    CAS  Article  PubMed  Google Scholar 

  67. Medina-Villar S, Alonso Á, Aldana BRV, Pérez-Corona E, Castro-Díez P (2015) Decomposition and biological colonization of native and exotic leaf litter in a Central Spain stream. Limnetica 34(2):293–310

    Google Scholar 

  68. Meneses DP, Gudiña EJ, Fernandes F, Gonçalves LRB, Rodrigues LR, Rodrigues S (2017) The yeast-like fungus Aureobasidium thailandense LB01 produces a new biosurfactant using olive oil mill wastewater as an inducer. Microbiol Res 204:40–47. https://doi.org/10.1016/j.micres.2017.07.004

    CAS  Article  PubMed  Google Scholar 

  69. Middelhoven WJ, Scorzetti G, Fell JW (2004) Systematics of the anamorphic basidiomycetous yeast genus Trichosporon Behrend with the description of five novel species: Trichosporon vadense, T. smithiae, T. dehoogii, T. scrabaeorum and T. gamsii. Int J Syst Evol Microbiol 54(3):975–986. https://doi.org/10.1099/ijs.0.02859-0

    CAS  Article  PubMed  Google Scholar 

  70. Molnár O, Wuczkowski M, Prillinger H (2008) Yeast biodiversity in the guts of several pests on maize; comparison of three methods: classical isolation, cloning and DGGE. Mycol Prog 7(2):111–123. https://doi.org/10.1007/s11557-008-0558-0

    Article  Google Scholar 

  71. Morais PB, Hagler AN, Rosa CA, Mendonça-Hagler LC, Klaczko LB (1992) Yeasts associated with Drosophila in tropical forests of Rio de Janeiro, Brazil. Can J Microbiol 38(11):1150–1155. https://doi.org/10.1139/m92-188

    CAS  Article  PubMed  Google Scholar 

  72. Morais PB, Rosa CA, Hagler AN, Mendonca-Hagler LC (1994) Yeast communities of the cactos Pilosocereus arrabidae as resources for larval and adult stages of Drosophila serido. Antonie Leeuwenhoek 66(4):313–317. https://doi.org/10.1007/BF00882766

    CAS  Article  PubMed  Google Scholar 

  73. Morais PB, Lachance MA, Rosa CA (2005) Saturnispora hagleri sp. nov., a yeast species isolated from Drosophila flies in Atlantic rainforest in Brazil. Int J Syst Evol Microbiol 55(4):1725–1727. https://doi.org/10.1099/ijs.0.63673-0

    CAS  Article  PubMed  Google Scholar 

  74. Morais CG, Cadete RM, Uetanabaro APT, Rosa LH, Lachance MA, Rosa CA (2013) D-xylose-fermenting and xylanase-producing yeast species from rotting wood of two Atlantic rainforest habitats in Brazil. Fungal Genet Biol 60:19–28. https://doi.org/10.1016/j.fgb.2013.07.003

    CAS  Article  PubMed  Google Scholar 

  75. Moubasher A, Abdel-Sater M, Soliman Z (2017) Yeasts and filamentous fungi inhabiting guts of three insect species in Assiut, Egypt. Mycosphere 8(9):1297–1316. https://doi.org/10.5943/mycosphere/8/9/4

    Article  Google Scholar 

  76. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(24):853–858. https://doi.org/10.1038/35002501

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. Nakase T, Suzuki M, Takashima M, Hamamoto M, Hatano T, Fukui S (1994) A taxonomic study on cellulolytic yeasts and yeast-like microorganisms isolated in Japan - I. Ascomycetous yeast genera Candida and Williopsis, and a yeast-like genus Prototheca. J Gen Appl Microbiol 40:519–531

    CAS  Article  Google Scholar 

  78. Nasanit R, Tangwong-O-Thai A, Tantirungkij M, Limtong S (2015) The assessment of epiphytic yeast diversity in sugarcane phyllosphere in Thailand by culture-independent method. Fungal Biol 119(12):1145–1157. https://doi.org/10.1016/j.funbio.2015.08.021

    Article  PubMed  Google Scholar 

  79. Nguyen NH, Suh S-O, Marshall CJ, Blackwell M (2006) Morphological and ecological similarities: wood-boring beetles associated with novel xylose-fermenting yeasts, Spathaspora passalidarum gen. sp nov and Candida jeffriesiisp nov. Mycol Res 110(10):1232–1241. https://doi.org/10.1016/j.mycres.2006.07.002

    Article  PubMed  Google Scholar 

  80. Nguyen NH, Suh S-O, Blackwell M (2007) Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99(6):842–858. https://doi.org/10.3852/mycologia.99.6.842

    CAS  Article  PubMed  Google Scholar 

  81. Noda H, Koizumi Y (2003) Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem Mol Biol 33(6):649–658. https://doi.org/10.1016/S0965-1748(03)00056-0

    CAS  Article  PubMed  Google Scholar 

  82. Oliveira JVC, Borges TA, Santos RAC, Freitas LFD, Rosa CA, Goldman GH, Riaño-Pachón DM (2014) Pseudozyma brasiliensis sp. nov., a xylanolytic, ustilaginomycetous yeast species isolated from an insect pest of sugarcane roots. Int J Syst Evol Microbiol 64:2159–2168. https://doi.org/10.1099/ijs.0.060103-0

    Article  PubMed  Google Scholar 

  83. Park JM, You Y-H, Back C-G, Kim H-H, Ghim SY, Park JH (2018) Fungal load in Bradysia agrestis, a phytopathogen-transmitting insect vector. Symbiosis 74(2):145–158. https://doi.org/10.1007/s13199017-0494-3

    Article  Google Scholar 

  84. Pes AMO, Hamada N, Nessimian JL (2005) Chaves de identificação de larvas para famílias e gêneros de trichoptera (Insecta) da Amazônia Central, Brasil. Rev Bras Entomol 49(2):181–204. https://doi.org/10.1590/S0085-56262005000200002

    Article  Google Scholar 

  85. Peterson SW, Manitchotpisit P, Leathers TD (2013) Aureobasidium thailandense sp. nov. isolated from leaves and wooden surfaces. Int J Syst Evol Microbiol 63:790–795. https://doi.org/10.1099/ijs.0.047613-0

    CAS  Article  PubMed  Google Scholar 

  86. Pimenta RS, Alves PDD, Almeida GMF, Silva JF, Morais PB, Corrêa A Jr, Rosa CA (2009) Yeast communities in two Atlantic rain Forest fragments in Southeast Brazil. Braz J Microbiol 40(1):90–95. https://doi.org/10.1590/S1517-83822009000100015

    Article  PubMed  PubMed Central  Google Scholar 

  87. Rao RS, Bhadra B, Shivaji S (2007) Isolation and characterization of xylitol-producing yeasts from the gut of colleopteran insects. Curr Microbiol 55(5):441–446. https://doi.org/10.1007/s00284-007-9005-8

    CAS  Article  PubMed  Google Scholar 

  88. Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado vegetation and threats to its biodiversity. Ann Bot 80:223–230. https://doi.org/10.1006/anbo.1997.0469

    Article  Google Scholar 

  89. Rezende RS, Sales MA, Hurbath F, Roque N, Gonçalves JF, Medeiros AO (2017) Effect of plant richness on the dynamics of coarse particulate organic matter in a Brazilian Savannah stream. Limnologica 63:57–64. https://doi.org/10.1016/j.limno.2017.02.002

    Article  Google Scholar 

  90. Ricci I, Damiani C, Scuppa P, Mosca M, Crotti E, Rossi P, Rizzi A, Capone A, Gonella E, Ballarini P, Chouaia B, Sagnon N, Esposito F, Alma A, Mandrioli M, Sacchi L, Bandi C, Daffonchio D, Favia G (2011) The yeast Wickerhamomyces anomalus (Pichia anomala) inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi. Environ Microbiol 13(4):911–921. https://doi.org/10.1111/j.14622920.2010.02395.x

    CAS  Article  PubMed  Google Scholar 

  91. Rivera FN, González E, Gómez Z, López N, Hernández-Rodríguez C, Berkov A, Zúñiga G (2009) Gut-associated yeast in bark beetles of the genus Dendroctonus Erichson (Coleoptera: Curculionidae: Scolytinae). Biol J Linnean Soc 98:325–342. https://doi.org/10.1111/j.1095-8312.2009.01289.x

    Article  Google Scholar 

  92. Rosa CA, Lachance MA, Silva JOC, Teixeira ACP, Marini MM, Antonini Y, Martins RP (2003) Yeast communities associated with stingless bees. FEMS Yeast Res 4(3):271–275. https://doi.org/10.1016/S1567-1356(03)00173-9

    CAS  Article  PubMed  Google Scholar 

  93. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  94. Santiago-Urbina JA, Peña-Montes C, Nolasco-Cancino H, Ruiz-Terán F (2016) Pcr-Dgge analysis of the yeast population associated with natural fermentation of Taberna. J Microbiol Biotechnol Food Sci 6(2):758–763. https://doi.org/10.15414/jmbfs.2016.6.2.758-763

    CAS  Article  Google Scholar 

  95. Sasaki T, Kawamura M, Ishikawa H (1996) Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J Insect Physiol 42(2):125–129. https://doi.org/10.1016/0022-1910(95)00086-0

    CAS  Article  Google Scholar 

  96. Schäfer A, Konrad R, Kuhnigk T, Kämpfer P, Hertel H, König H (1996) Hemicellulose degrading bacteria and yeasts from the termite gut. J Appl Bacteriol 80(5):471–478

    Article  Google Scholar 

  97. Shannon C (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423, 623–656

    Article  Google Scholar 

  98. Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanová L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16(1):49–67. https://doi.org/10.1007/s10531-006-9120-z

    Article  Google Scholar 

  99. Silva-Bedoya LM, Ramírez-Castrillón M, Osorio-Cadavid E (2014) Yeast diversity associated to sediments and water from two Colombian artificial lakes. Braz J Microbiol 45(1):135–142. https://doi.org/10.1590/S1517-83822014005000035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  100. Simpson E (1949) Measurement of diversity. Nature 163:688. https://doi.org/10.1038/163688a0

    Article  Google Scholar 

  101. Siri A, Lastra CCL (2010) Diversity of trichomycetes in larval flies from aquatic habitats in Argentina. Mycologia 102(2):347–362. https://doi.org/10.3852/08-103

    Article  PubMed  Google Scholar 

  102. Sirot LK, Hardstone MC, Helinski MEH, Ribeiro JMC, Kimura M, Deewatthanawong P, Wolfner MF, Harrington LC (2011) Towards a semen proteome of the dengue vector mosquito: protein identification and potential functions. PLoS Negl Trop Dis 5(3):1–11. https://doi.org/10.1371/journal.pntd.0000989

    CAS  Article  Google Scholar 

  103. Stefani FOP, Klimaszewski J, Morency M-J, Bourdon C, Labrie P, Blais M, Venier L, Séguin A (2016) Fungal community composition in the gut of rove beetles (Coleoptera: Staphylinidae) from the Canadian boreal forest reveals possible endosymbiotic interactions for dietary needs. Fungal Ecol 23:164–171. https://doi.org/10.1016/j.funeco.2016.05.001

    Article  Google Scholar 

  104. Steyn A, Roets F, Botha A (2016) Yeasts associated with Culex pipiens and Culex theileri mosquito larvae and the effect of selected yeast strains on the ontogeny of Culex pipiens. Microb Ecol 71(3):747–760. https://doi.org/10.1007/s00248-015-0709-1

    CAS  Article  PubMed  Google Scholar 

  105. Strauss MLA, Jolly NP, Lambrechts MG, Rensburg PV (2001) Screening for the production of extracellular hydrolytic enzymes by non- Saccharomyces wine yeasts. J Appl Microbiol 91:182–190. https://doi.org/10.1046/j.1365-2672.2001.01379.x

    CAS  Article  PubMed  Google Scholar 

  106. Suh SO, Zhou JJ (2011) Kazachstania intestinalis sp. nov., an ascosporogenous yeast from the gut of passalid beetle Odontotaenius disjunctus. Anton Leeuw Int J G 100(1):109–115. https://doi.org/10.1007/s10482-011-9569-y

    Article  Google Scholar 

  107. Suh S-O, Marshall C, McHugh JV, Blackwell M (2003) Wood ingestion by passalid beetles in the presence of xylose-fermenting gut yeasts. Mol Ecol 12(11):3137–3145. https://doi.org/10.1046/j.1365294X.2003.01973.x

    Article  PubMed  Google Scholar 

  108. Suh S-O, McHugh JV, Pollock DD, Blackwell M (2005) The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109(3):261–265. https://doi.org/10.1017/S0953756205002388

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  109. Suh S-O, 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. https://doi.org/10.1111/j.1567-1364.2007.00320.x

    CAS  Article  PubMed  Google Scholar 

  110. Suh S-O, Houseknecht JL, Gujjari P, Zhou JJ (2013) Scheffersomyces parashehatae f.a., sp. nov., Scheffersomyces xylosifermentans f.a., sp. nov., Candida broadrunensis sp. nov. and Candida manassasensis sp. nov., novel yeasts associated with wood-ingesting insects, and their ecological and biofuel implications. Int J Syst Evol Microbiol 63(11):4330–4339. https://doi.org/10.1099/ijs.0.053009-0

    CAS  Article  PubMed  Google Scholar 

  111. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  112. Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. J N Am Benthol Soc 29(1):118–146. https://doi.org/10.1899/08-170.1

    Article  Google Scholar 

  113. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/nar/22.22.4673

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  114. Thongekkaew J, Ikeda H, Masaki K, Iefuji H (2008) An acidic and thermostable carboxymethyl cellulase from the yeast Cryptococcus sp. S-2: purification, characterization and improvement of its recombinant enzyme production by high cell-density fermentation of Pichia pastoris. Protein Expr Purif 60(2):140–146. https://doi.org/10.1016/j.pep.2008.03.021

    CAS  Article  PubMed  Google Scholar 

  115. 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. https://doi.org/10.1016/j.funeco.2013.06.005

    Article  Google Scholar 

  116. Urubschurov V, Janczyk P (2011) Biodiversity of yeasts in the gastrointestinal ecosystem with emphasis on its importance for the host. In: Grillo O, Venora G (eds) The dynamical processes of biodiversity-case studies of evolution and spatial distribution. InTech, Rijeka, pp 277–302

    Google Scholar 

  117. White MM, Lichtwardt RW (2004) Fungal symbionts (Harpellales) in Norwegian aquatic insect larvae. Mycologia 96(4):891–910. https://doi.org/10.2307/3762122

    Article  PubMed  Google Scholar 

  118. Yamoah E, Jones EE, Weld RJ, Suckling DM, Waipara N, Bourdôt GW, Hee AKW, Stewart A (2008) Microbial population and diversity on the exoskeletons of four insect species associated with gorse (Ulex europaeus L.). Aust J Entomol 47(4):370–379. https://doi.org/10.1111/j.1440-6055.2008.00655.x

    Article  Google Scholar 

  119. Yun YH, Suh DY, Yoo HD, Oh MH, Kim SH (2015) Yeast associated with the ambrosia beetle, Platypus koryoensis, the pest of oak trees in Korea. Mycobiology 43(4):458–466. https://doi.org/10.5941/MYCO.2015.43.4.458

    Article  PubMed  PubMed Central  Google Scholar 

  120. Yurkov AM, Kemler M, Begerow D (2011) Species accumulation curves and incidence-based species richness estimators to appraise the diversity of cultivable yeasts from beech forest soils. PLoS One 6(8):1–9. https://doi.org/10.1371/journal.pone.0023671

    CAS  Article  Google Scholar 

  121. Yurkov AM, Röhl O, Pontes A, Carvalho C, Maldonado C, Sampaio JP (2015) Local climatic conditions constrain soil yeast diversity patterns in Mediterranean forests, woodlands and scrub biome. FEMS Yeast Res 16(1):1–11. https://doi.org/10.1093/femsyr/fov103

    CAS  Article  Google Scholar 

  122. Zacchi L, Vaughan-Martini A (2002) Yeasts associated with insects in agricultural areas of Perugia, Italy. Ann Microbiol 52:237–244

    Google Scholar 

  123. Zhang N, Suh S-O, Blackwell M (2003) Microorganisms in the gut of beetles: evidence from molecular cloning. J Invertebr Pathol 84(3):226–233. https://doi.org/10.1016/j.jip.2003.10.002

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This research was supported by grant 407676/2013-9 from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Edital Chamada MCTI/CNPq/FNDCT Ação Transversal - Redes Regionais de Pesquisa em Ecossistemas, Biodiversidade e Biotecnologia N ° 79/2013.

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dos Santos, T.T., de Oliveira, D.P., Cabette, H.S.R. et al. The digestive tract of Phylloicus (Trichoptera: Calamoceratidae) harbours different yeast taxa in Cerrado streams, Brazil. Symbiosis 77, 147–160 (2019). https://doi.org/10.1007/s13199-018-0577-9

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Keywords

  • Aquatic macroinvertebrates
  • Freshwater
  • Fungal diversity, fungus-insect interaction
  • Symbiosis