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Yeast communities associated with ectomycorrhizal fungi in different Nothofagus forests of northwestern Patagonia

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A Correction to this article was published on 01 February 2022

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Abstract

Many surveys have studied soil yeasts and ectomycorrhizal fungi independently and reported their association with water availability and soil nutrients. Nevertheless, the importance of yeasts associated with ectomycorrhizal fungi and different exploration types is little understood. The aim of the present study is to describe the diversity of yeasts inhabiting the ectomycorrhizosphere, and their association with the ectomycorrhizal fungal community, in four Nothofagus forests in northwestern Patagonia. Most ectomycorrhizal fungi sequences were assigned to eight ectomycorrhizal lineages, a high percentage of which were related to /cortinarius lineage. Less than 25% of these sequences were associated with /non-ectomycorrhizal lineages reported as endophytic fungi. A large proportion of the sequences (81%) corresponded to the phylum Basidiomycota, and included the cosmopolitan genera Cortinarius, Inocybe and Tomentella. Three exploratory types were present in all forest sites, but with different distributions. The results showed that the ectomycorrhizal yeast communities were very diverse in the four forest sites studied. Ectomycorrhizospheric yeasts were also dominated by the phylum Basidiomycota, including the genera Naganishia, Solicoccozyma, Saitozyma and Piskurozyma. The species Apiotrichum porossum, Solicoccozyma podzolica, Solicoccozyma terricola, Solicoccozyma sp. and Humicolopsis cephalosporioides were frequently associated with EcM fungal species. The distribution and diversity of the ectomycorrhizospheric yeast species suggest a different community to that of the bulk-soil and rhizosphere of previously reported Nothofagus native forests, which could be related to exudation and nutrient availability, as well as environmental features. The data reported here are relevant for disturbance (natural and human-related) and management studies on Nothofagus forests.

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References

  • Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V et al (2010) PlutoF—a web based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences. Evol Bioinformatics Online 6:189–196

    Google Scholar 

  • Acosta MC, Premoli AC (2010) Evidence of chloroplast capture in south American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol Phylogenet Evol 54:235–242

    PubMed  Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:07–114

    Google Scholar 

  • Agerer R (1997) Colour atlas of ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger GmbH

  • Azpilicueta M, Pastorino M, Puntieri J, Barbero F, Martinez-Meier A, Marchelli P, Gallo L (2014) Robles in Lagunas de Epulauquen, Argentina: previous and recent evidence of their distinctive character. Rev Chil Hist Nat 87:1–12

    Google Scholar 

  • Barroetaveña C, Salomón MES, Bassani V (2019) Rescuing the ectomycorrhizal biodiversity associated with south American Nothofagaceae forest, from the 19th century naturalists up to molecular biogeography. For An Int J For Res 92:500–511

    Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    PubMed  Google Scholar 

  • Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem.43: −8

  • Bruzone MC, Fehrer J, Fontenla SB, Vohník M (2017) First record of Rhizoscyphus ericae in southern Hemisphere’s Ericaceae. Mycorrhiza 27:147–163

    PubMed  Google Scholar 

  • Bruzone MC, Fontenla S, Vohník M (2015) Is the prominent ericoid mycorrhizal fungus Rhizoscyphus ericae absent in the southern Hemisphere’s Ericaceae? A case study on the diversity of root mycobionts in Gaultheria spp. from Northwest Patagonia, Argentina. Mycorrhiza 25:25–40

    PubMed  Google Scholar 

  • Carron AI, Garibaldi LA, Marquez S, Fontenla S (2020) The soil fungal community of native woodland in Andean Patagonian forest: a case study considering experimental forest management and seasonal effects. For Ecol Manag 461:117955

    Google Scholar 

  • Cavello IA, Bezus B, Martinez A, Garmendia G, Vero S, Cavalitto S (2019) Yeasts from Tierra Del Fuego Province (Argentina): biodiversity, characterization and bioprospection of hydrolytic enzymes. Geomicrobiol J 36:47–857

    Google Scholar 

  • de García V, Brizzio S, Libkind D, Rosa CA, van Broock M (2010) Wickerhamomyces patagonicus sp. nov., an ascomycetous yeast species from Patagonia, Argentina. Int J Syst Evol Microbiol 60:1693–1696

    PubMed  Google Scholar 

  • Defrenne CE, Philpott TJ, Guichon SHA, Roach WJ, Pickles BJ, Simard SW (2019) Shifts in ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior Douglas-fir forests of Western Canada. Front Plant Sci 10

  • Dickie IA, Bolstridge N, Cooper JA, Peltzer DA (2010) Co-invasion by Pinus and its mycorrhizal fungi. New Phytol 187:475–484

    PubMed  Google Scholar 

  • Diehl P, Mazzarino MJ, Fontenla S (2008) Plant limiting nutrients in Andean-Patagonian woody species: effects of interannual rainfall variation, soil fertility and mycorrhizal infection. For Ecol Manag 255:2973–2980

    Google Scholar 

  • Donoso Zegers C (2006) Las especies arbóreas de los bosques templados de Chile y Argetina. Autoecologı́a, Marisa Cuneo Ediciones, Valdivia, Chile

  • Duo Saito RA, Connell L, Rodriguez R, Redman R, Libkind D, de Garcia V (2018) Metabarcoding analysis of the fungal biodiversity associated with Castaño Overa glacier – mount Tronador, Patagonia, Argentina. Fungal Ecol 36:1–16

    Google Scholar 

  • El-Tarabily KA, Sivasithamparam K (2006) Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 47:5–35

    Google Scholar 

  • Elíades LA, Cabello MN, Pancotto V, Moretto A, Rago MM, Saparrat MCN (2015) Preliminary data on growth and enzymatic abilities of soil fungus Humicolopsis cephalosporioides at different incubation temperatures. Rev Iberoam Micol 32:40–45

    PubMed  Google Scholar 

  • Erlandson S, Wei X, Savage J, Cavender‐Bares J Peay K (2018) Soil abiotic variables are more important than Salicaceae phylogeny or habitat specialization in determining soil microbial community structure. Mol Ecol 27:2007–2024.

  • Fernández N, Marchelli P, Fontenla S (2013) Ectomycorrhizas naturally established in Nothofagus nervosa seedlings under different cultivation practices in a forest nursery. Microb Ecol 66:581–592

    PubMed  Google Scholar 

  • Fernández NV, Fontenla SB, Moguilevsky D, Meie S, Rilling J, Cornejo P (2018) Nothofagus pumilio forest affected by recent tephra deposition in northern Patagonia. II-Shifts in diversity and structure of rhizosphere fungal communities J Soil Sci Plant Nutr 18:499–511

    Google Scholar 

  • Fernández NV, Marchelli P, Gherghel F, Kost G, Fontenla SB (2015) Ectomycorrhizal fungal communities in Nothofagus nervosa (Raulí): a comparison between domesticated and naturally established specimens in a native forest of Patagonia, Argentina. Fungal Ecol 18:36–47

    Google Scholar 

  • Fernández NV, Mestre MC, Marchelli P, Fontenla SB (2012) Yeast and yeast-like fungi associated with dry indehiscent fruits of a tree species in Patagonia, Argentina. FEMS Microbiol Ecol 80:179–192

    PubMed  Google Scholar 

  • Fracchia S, Godeas A, Scervino JM, Sampedro I, Ocampo JA, Garcıa-Romera I (2003) Interaction between the soil yeast Rhodotorula mucilaginosa and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Soil Biol Biochem 35:701–707

    CAS  Google Scholar 

  • Garbaye J, Bowen GD (1989) Stimulation of ectomycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388

    Google Scholar 

  • Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26:6960–6973.

  • Glushakova AM, Kachalkin AV, Tiunov AV, Chernov IY (2017) Distribution of yeast complexes in the profiles of different soil types. Eurasian Soil Sci 50:820–825

    CAS  Google Scholar 

  • Hewitt RE, Taylor DL, Hollingsworth TN, Anderson CB, Martínez Pastur G (2018) Variable retention harvesting influences belowground plant-fungal interactions of Nothofagus pumilio seedlings in forests of southern Patagonia. PeerJ 6:5008

    Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    PubMed  Google Scholar 

  • Kuhar F, Barroetaveña C, Rajchenberg M (2016) New species of Tomentella (Thelephorales) from the Patagonian Andes forests. Mycologia 108:780–790

    CAS  PubMed  Google Scholar 

  • Kuhar F, Smith ME, Mujic A, Truong C, Nouhra E (2017) A systematic overview of Descolea (Agaricales) in the Nothofagaceae forests of Patagonia. Fungal Biol 121:876–889

    PubMed  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Soft 25:1–18

    Google Scholar 

  • Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J, Johnston et al (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Nat Acad Sci 108:14539–14544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Libkind D, Moliné M, Sampaio J, van Broock M (2009) Yeast from high altitude lakes: influence of UV radiation. FEMS Microbiol Ecol 69:353–362

    CAS  PubMed  Google Scholar 

  • Marchand S (1976) Tres géneros de Hifomicetes de Tierra del Fuego. Bol Soc. Arg Bot 17:63–72

    Google Scholar 

  • Mašínová T, Yurkov A, Baldrian P (2018) Forest soil yeasts: decomposition potential and the utilization of carbon sources. Fungal Ecol 34:10–19

    Google Scholar 

  • Mello A, Murat C, Bonfante P (2006) Truffles: much more than a prized and local fungal delicacy. FEMS Microbiol Lett 260:1–8

    CAS  PubMed  Google Scholar 

  • Mestre MC, Fontenla S, Bruzone MC, Fernández NV, Dames J (2016) Detection of plant growth enhancing features in psychrotolerant yeasts from Patagonia (Argentina). J Basic Microbiol 56:1098–1106

    CAS  PubMed  Google Scholar 

  • Mestre MC, Fontenla S, Rosa CA (2014) Ecology of cultivable yeasts in pristine forests in northern Patagonia (Argentina) influenced by different environmental factors. Can J Microbiol 60:371–382

    CAS  PubMed  Google Scholar 

  • Mestre MC, Libkind D, Fontenla S (2009) Comparación de condiciones de cultivo para el aislamiento y recuento simultáneo de levaduras de suelos de bosques nativos de Nothofagus spp. (Fagaceae) de la Patagonia Argentina. Bol Soc Arg Bot 44:229–238

    Google Scholar 

  • Mestre MC, Pastorino MJ, Aparicio AG, Fontenla SB (2017) Natives helping foreigners?: the effect of inoculation of poplar with patagonian beneficial microorganisms. J Soil Sci Plant Nutr 17:1028–1039

    CAS  Google Scholar 

  • Mestre MC, Rosa CA, Safar SVB, Libkind D, Fontenla SB (2011) Yeast communities associated with the bulk-soil, rhizosphere and ectomycorrhizosphere of a Nothofagus pumilio forest in northwestern Patagonia, Argentina. FEMS Microbiol Ecol 78:31–541

    Google Scholar 

  • Mestre MC, Ulloa JR, Rosa CA, Lachance MA, Fontenla S (2010) Lachancea nothofagi sp. nov., a yeast associated with Nothofagus species in Patagonia, Argentina. Int J Syst Evol Microbiol 60:2247–2250

    CAS  PubMed  Google Scholar 

  • Moguilevsky D, Fernández NV, Cornejo PE, Puntieri JG and Fontenla SB (2018) Nothofagus pumilio forest affected by recent tephra deposition in northern Patagonia. I- environmental traits influencing seedling growth. J soil Sci plant Nutr 0–0

  • Nouhra E, Urcelay C, Longo S, Tedersoo L (2013) Ectomycorrhizal fungal communities associated to Nothofagus species in northern Patagonia. Mycorrhiza 23:487–496

    PubMed  Google Scholar 

  • Nouhra ER, Urcelay C, Longo MS, Fontenla S (2012) Differential hypogeous sporocarp production from Nothofagus dombeyi and N. pumilio forests in southern Argentina. Mycologia 104:45–52. https://doi.org/10.3852/11-098

    Article  PubMed  Google Scholar 

  • Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P (2019) McGlinn 439 D et al. Vegan Community Ecol Packag R Packag version:2–5

  • Pastor N, Chiapella J, Kuhar F, Mujic AB, Crespo EM, Nouhra ER (2019) Unveiling new sequestrate Cortinarius species from northern Patagonian Nothofagaceae forests based on molecular and morphological data. Mycologia 111:103–117

    CAS  PubMed  Google Scholar 

  • Salgado Salomón ME, Dresch P, Horak E, Galleguillos F, Barroetaveña C, Peintner U (2018) The enigmatic Cortinarius magellanicus complex occurring in Nothofagaceae forests of the southern hemisphere. Fungal Biol 122:1077–1097

    PubMed  Google Scholar 

  • San-Fabian B, Niskanen T, Liimatainen K, Kooij PW, Mujic AB, Truong C, Peintner U, Dresch P, Nouhra E, Matheny PB, Smith ME (2018) New species of Cortinarius sect. Austroamericani, sect. Nov., from south American Nothofagaceae forests. Mycologia 110:1127–1144

    CAS  PubMed  Google Scholar 

  • Soteras F, Ibarra C, Geml J, Barrios-García MN, Domínguez LS, Nouhra ER (2017) Mycophagy by invasive wild boar (Sus scrofa) facilitates dispersal of native and introduced mycorrhizal fungi in Patagonia, Argentina. Fungal Ecol 26:51–58

    Google Scholar 

  • Taniguchi T, Kitajima K, Douhan GW, Yamanaka N, Allen MF (2018) A pulse of summer precipitation after the dry season triggers changes in ectomycorrhizal formation, diversity, and community composition in a Mediterranean forest in California, USA. Mycorrhiza 28:665–677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 80:367

    Google Scholar 

  • Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11:3166–3178

    CAS  PubMed  Google Scholar 

  • Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99

    Google Scholar 

  • Truong C, Gabbarini L, Corrales A, Mujic A, Escobar J, Moretto A, Smith M (2019) Ectomycorrhizal fungi and soil enzymes exhibit contrasting patterns along elevation gradients in southern Patagonia. New Phytol 222:1936–1950

    CAS  PubMed  Google Scholar 

  • Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval-Leiva PA, Fernández N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sánchez-García M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214:913–919

    PubMed  Google Scholar 

  • Vohnik M, Fendrych M, Kolarik M, Gryndler M, Hrrselova H, Albrechtova J, Vosatka M (2007) The ascomycete Meliniomyces variabilis isolated from a sporocarp of Hydnotrya tulasnei (Pezizales) intracellularly colonizes roots of ecto-and ericoid mycorrhizal host plants. Czech Mycol 59:215–226

    Google Scholar 

  • Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol 164:7–10

    PubMed  Google Scholar 

  • Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154

    CAS  PubMed  Google Scholar 

  • Yurkov A, Krüger D, Begerow D, Arnold N, Tarkka MT (2012) Basidiomycetous yeasts from Boletales fruiting bodies and their interactions with the mycoparasite Sepedonium chrysospermum and the host fungus Paxillus. Microb Ecol 63:295–303

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zacchi L, Vaughan-Martini A, Angelini P (2003) Yeast distribution in a truffle-field ecosystem. Ann Microbiol 53:275–282

    Google Scholar 

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Acknowledgements

We wish to thank the authorities of Administración de Parques Nacionales (Argentina) for their courtesy and cooperation (permit 1280, 2008). We thank BSc. (Hons) Audrey Urquhart for language revision. This work was supported by project UNComahue (B200), FONCyT projects PICT04-22200 and PICT2014-1839.

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This work was supported by project UNComahue (B200), FONCyT projects PICT04–22200 and PICT2014–1839.

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  1. IPATEC (Universidad Nacional del Comahue-CONICET), Bariloche, Río Negro, Argentina

    M. Cecilia Mestre

  2. Laboratorio de Microbiología Aplicada y Biotecnología, Centro Regional Universitario Bariloche (CRUB), Universidad Nacional del Comahue (UNCO), Bariloche, Río Negro, Argentina

    M. Cecilia Mestre & Sonia Fontenla

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  1. M. Cecilia Mestre
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Correspondence to M. Cecilia Mestre.

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Mestre, M.C., Fontenla, S. Yeast communities associated with ectomycorrhizal fungi in different Nothofagus forests of northwestern Patagonia. Symbiosis 84, 179–193 (2021). https://doi.org/10.1007/s13199-021-00782-4

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