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Towards understanding diversity, endemicity and global change vulnerability of soil fungi

View ORCID ProfileLeho Tedersoo, Vladimir Mikryukov, Alexander Zizka, Mohammad Bahram, Niloufar Hagh-Doust, View ORCID ProfileSten Anslan, Oleh Prylutskyi, Manuel Delgado-Baquerizo, Fernando T. Maestre, Jaan Pärn, Maarja Öpik, Mari Moora, Martin Zobel, Mikk Espenberg, Ülo Mander, Abdul Nasir Khalid, Adriana Corrales, Ahto Agan, Aída-M. Vasco-Palacios, Alessandro Saitta, Andrea C. Rinaldi, Annemieke Verbeken, Bobby P. Sulistyo, Boris Tamgnoue, Brendan Furneaux, View ORCID ProfileCamila Duarte Ritter, Casper Nyamukondiwa, Cathy Sharp, César Marín, Daniyal Gohar, Darta Klavina, Dipon Sharmah, Dong Qin Dai, Eduardo Nouhra, Elisabeth Machteld Biersma, Elisabeth Rähn, Erin K. Cameron, Eske De Crop, Eveli Otsing, Evgeny A. Davydov, Felipe E. Albornoz, Francis Q. Brearley, Franz Buegger, Geoffrey Zahn, Gregory Bonito, Inga Hiiesalu, Isabel C. Barrio, Jacob Heilmann-Clausen, Jelena Ankuda, John Y. Kupagme, Jose G. Maciá-Vicente, Joseph Djeugap Fovo, József Geml, Juha M. Alatalo, Julieta Alvarez-Manjarrez, Kadri Põldmaa, Kadri Runnel, Kalev Adamson, View ORCID ProfileKari Anne Bråthen, Karin Pritsch, Kassim I. Tchan, Kęstutis Armolaitis, Kevin D. Hyde, Kevin K. Newsham, Kristel Panksep, Adebola A. Lateef, Liis Tiirmann, Linda Hansson, Louis J. Lamit, Malka Saba, View ORCID ProfileMaria Tuomi, Marieka Gryzenhout, Marijn Bauters, Meike Piepenbring, Nalin Wijayawardene, Nourou S. Yorou, Olavi Kurina, Peter E. Mortimer, Peter Meidl, Petr Kohout, R. Henrik Nilsson, Rasmus Puusepp, Rein Drenkhan, Roberto Garibay-Orijel, Roberto Godoy, Saad Alkahtani, Saleh Rahimlou, Sergey V. Dudov, Sergei Põlme, Soumya Ghosh, Sunil Mundra, Talaat Ahmed, Tarquin Netherway, Terry W. Henkel, Tomas Roslin, Vincent Nteziryayo, Vladimir E. Fedosov, Vladimir G. Onipchenko, W. A. Erandi Yasanthika, Young Woon Lim, Nadejda A. Soudzilovskaia, Alexandre Antonelli, Urmas Kõljalg, Kessy Abarenkov
doi: https://doi.org/10.1101/2022.03.17.484796
Leho Tedersoo
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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  • ORCID record for Leho Tedersoo
  • For correspondence: leho.tedersoo@ut.ee
Vladimir Mikryukov
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Alexander Zizka
3Department of Biology, Philipps-University, Marburg, Germany
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Mohammad Bahram
4Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
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Niloufar Hagh-Doust
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Sten Anslan
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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  • ORCID record for Sten Anslan
Oleh Prylutskyi
5Department of Mycology and Plant Resistance, School of Biology, V.N. Karazin Kharkiv National University, Kharkiv, Ukraine
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Manuel Delgado-Baquerizo
6Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain
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Fernando T. Maestre
7Instituto Multidisciplinar para el Estudio del Medio ‘Ramón Margalef’ and Departamento de Ecología, Universidad de Alicante; 03690, Alicante, Spain
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Jaan Pärn
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Maarja Öpik
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Mari Moora
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Martin Zobel
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Mikk Espenberg
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Ülo Mander
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Abdul Nasir Khalid
8Institute of Botany, University of the Punjab, Lahore, Pakistan
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Adriana Corrales
9Centro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Universidad del Rosario, Bogotá, Colombia
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Ahto Agan
10Institute of Forestry and Engineering, Estonian University of Life Sciences, Tartu, Estonia
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Aída-M. Vasco-Palacios
11Escuela de Microbiologia, Universidad de Antioquia, Medellin, Antioquia, Colombia
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Alessandro Saitta
12Department of Agricultural, Food and Forest Sciences, University of Palermo, Palermo, Italy
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Andrea C. Rinaldi
13Department of Biomedical Sciences, University of Cagliari, Cagliari, Italy
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Annemieke Verbeken
14Department Biology, Ghent University, Ghent, Belgium
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Bobby P. Sulistyo
15Department of Biomedicine, Indonesia International Institute for Life Sciences, Jakarta, Indonesia
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Boris Tamgnoue
16Department of Crop Science, University of Dschang, Dschang, Cameroon
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Brendan Furneaux
17Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden
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Camila Duarte Ritter
18Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, PR, Brazil
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Casper Nyamukondiwa
19Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana
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Cathy Sharp
20Natural History Museum of Zimbabwe, Bulawayo, Zimbabwe
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César Marín
21Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Universidad SantoTomás, Santiago, Chile
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Daniyal Gohar
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Darta Klavina
22Latvian State Forest Research Insitute Silava, Salaspils, Latvia
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Dipon Sharmah
23Department of Botany, Jawaharlal Nehru Rajkeeya Mahavidyalaya, Pondicherry University, Port Blair, India
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Dong Qin Dai
24College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan, China
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Eduardo Nouhra
25Instituto Multidisciplinario de Biología Vegetal (CONICET), Universidad Nacional de Córdoba, Cordoba, Argentina
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Elisabeth Machteld Biersma
26Natural History Museum of Denmark, Copenhagen, Denmark
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Elisabeth Rähn
10Institute of Forestry and Engineering, Estonian University of Life Sciences, Tartu, Estonia
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Erin K. Cameron
27Department of Environmental Science, Saint Mary’s University, Halifax, Nova Scotia, Canada
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Eske De Crop
14Department Biology, Ghent University, Ghent, Belgium
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Eveli Otsing
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Evgeny A. Davydov
28Altai State University, Barnaul, Russia
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Felipe E. Albornoz
29CSIRO Land and Water, Wembley, WA, Australia
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Francis Q. Brearley
30Department of Natural Sciences, Manchester Metropolitan University, Manchester, UK
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Franz Buegger
31Helmholtz Zentrum München, Neuherberg, Germany
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Geoffrey Zahn
32Utah Valley University, Orem UT, USA
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Gregory Bonito
33Plant, Soil and Microbial Sciences, Michigan State University, East Lansing MI, USA
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Inga Hiiesalu
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Isabel C. Barrio
34Faculty of Natural and Environmental Sciences, Agricultural University of Iceland, Hvanneyri, Iceland
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Jacob Heilmann-Clausen
35Center for Macroecology, Evolution and Climate, University of Copenhagen, Copenhagen, Denmark
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Jelena Ankuda
36Department of Silviculture and Ecology, Institute of Forestry of Lithuanian Research Centre for Agriculture and Forestry (LAMMC). Girionys, Lithuania
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John Y. Kupagme
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Jose G. Maciá-Vicente
37Plant Ecology and Nature Conservation, Wageningen University & Research, Wageningen, The Netherlands
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Joseph Djeugap Fovo
16Department of Crop Science, University of Dschang, Dschang, Cameroon
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József Geml
38ELKH-EKKE Lendület Environmental Microbiome Research Group, Eszterházy Károly Catholic University, Eger, Hungary
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Juha M. Alatalo
39Environmental Science Center, Qatar University, Doha, Qatar
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Julieta Alvarez-Manjarrez
40Biology Department, Stanford University, Stanford CA, USA
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Kadri Põldmaa
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Kadri Runnel
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Kalev Adamson
10Institute of Forestry and Engineering, Estonian University of Life Sciences, Tartu, Estonia
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Kari Anne Bråthen
41Department of Arctic and Marine Biology, The Arctic University of Norway, Tromsø, Norway
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Karin Pritsch
31Helmholtz Zentrum München, Neuherberg, Germany
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Kassim I. Tchan
42Research Unit Tropical Mycology and Plants-Soil Fungi Interactions, University of Parakou, Parakou, Benin
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Kęstutis Armolaitis
36Department of Silviculture and Ecology, Institute of Forestry of Lithuanian Research Centre for Agriculture and Forestry (LAMMC). Girionys, Lithuania
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Kevin D. Hyde
43Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, Thailand
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Kevin K. Newsham
44NERC British Antarctic Survey, High Cross, Cambridge, UK
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Kristel Panksep
45Chair of Hydrobiology and Fishery, Estonian University of Life Sciences, Tartu, Estonia
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Adebola A. Lateef
46Department of Plant Biology, University of Ilorin, Ilorin, Nigeria
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Liis Tiirmann
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Linda Hansson
47Gothenburg Centre for Sustainable Development, Gothenburg, Sweden
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Louis J. Lamit
48Department of Biology, Syracuse University, Syracuse NY, USA
49Department of Environmental and Forest Biology, State University of New York College of Environmental Science and Forestry, Syracuse NY, USA
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Malka Saba
50Department of Plant Sciences, Quaid-i-Azam University, Islamabad, Pakistan
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Maria Tuomi
41Department of Arctic and Marine Biology, The Arctic University of Norway, Tromsø, Norway
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Marieka Gryzenhout
51Department of Genetics, University of the Free State, Bloemfontein, South Africa
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Marijn Bauters
52Department of Environment, Ghent University, Ghent, Belgium
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Meike Piepenbring
53Mycology Working Group, Goethe University Frankfurt am Main, Frankfurt am Main, Germany
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Nalin Wijayawardene
24College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan, China
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Nourou S. Yorou
42Research Unit Tropical Mycology and Plants-Soil Fungi Interactions, University of Parakou, Parakou, Benin
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Olavi Kurina
54Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia
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Peter E. Mortimer
55Center For Mountain Futures, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
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Peter Meidl
56Freie Universität Berlin, Institut für Biologie, Berlin, Germany
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Petr Kohout
57Institute of Microbiology, Czech Academy of Sciences, Prague, Czech Republic
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R. Henrik Nilsson
58Gothenburg Global Biodiversity Centre, University of Gothenburg, Gothenburg, Sweden
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Rasmus Puusepp
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Rein Drenkhan
10Institute of Forestry and Engineering, Estonian University of Life Sciences, Tartu, Estonia
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Roberto Garibay-Orijel
59Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, México
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Roberto Godoy
60Instituto Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile
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Saad Alkahtani
61College of Science, King Saud University, Riyadh, Saudi Arabia
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Saleh Rahimlou
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Sergey V. Dudov
62Department of Ecology and Plant Geography, Moscow Lomonosov State University, Moscow, Russia
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Sergei Põlme
1Center of Mycology and Microbiology, University of Tartu, Tartu, Estonia
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Soumya Ghosh
51Department of Genetics, University of the Free State, Bloemfontein, South Africa
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Sunil Mundra
63Department of Biology, College of Science, United Arab Emirates University, Abu Dhabi, UAE
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Talaat Ahmed
39Environmental Science Center, Qatar University, Doha, Qatar
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Tarquin Netherway
4Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
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Terry W. Henkel
64Department of Biological Sciences, California State Polytechnic University, Arcata CA, USA
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Tomas Roslin
4Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
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Vincent Nteziryayo
65Department of Food Science and Technology, University of Burundi, Bujumbura, Burundi
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Vladimir E. Fedosov
62Department of Ecology and Plant Geography, Moscow Lomonosov State University, Moscow, Russia
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Vladimir G. Onipchenko
62Department of Ecology and Plant Geography, Moscow Lomonosov State University, Moscow, Russia
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W. A. Erandi Yasanthika
43Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, Thailand
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Young Woon Lim
66School of Biological Sciences and Institute of Microbiology, Seoul National University, Seoul, Korea
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Nadejda A. Soudzilovskaia
67Centre for Environmental Sciences, Hasselt University, Hasselt, Belgium
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Alexandre Antonelli
68Royal Botanic Gardens, Kew, Richmond, United Kingdom
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Urmas Kõljalg
2Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
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Kessy Abarenkov
69University of Tartu Natural History Museum, Tartu, Estonia
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  • Abstract
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Summary

Fungi play pivotal roles in ecosystem functioning, but little is known about their global patterns of diversity, endemicity, vulnerability to global change drivers and conservation priority areas. We applied the high-resolution PacBio sequencing technique to identify fungi based on a long DNA marker that revealed a high proportion of hitherto unknown fungal taxa. We used a Global Soil Mycobiome consortium dataset to test relative performance of various sequencing depth standardization methods (calculation of residuals, exclusion of singletons, traditional and SRS rarefaction, use of Shannon index of diversity) to find optimal protocols for statistical analyses. Altogether, we used six global surveys to infer these patterns for soil-inhabiting fungi and their functional groups. We found that residuals of log-transformed richness (including singletons) against log-transformed sequencing depth yields significantly better model estimates compared with most other standardization methods. With respect to global patterns, fungal functional groups differed in the patterns of diversity, endemicity and vulnerability to main global change predictors. Unlike α-diversity, endemicity and global-change vulnerability of fungi and most functional groups were greatest in the tropics. Fungi are vulnerable mostly to drought, heat, and land cover change. Fungal conservation areas of highest priority include wetlands and moist tropical ecosystems.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 19, 2022.
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Towards understanding diversity, endemicity and global change vulnerability of soil fungi
Leho Tedersoo, Vladimir Mikryukov, Alexander Zizka, Mohammad Bahram, Niloufar Hagh-Doust, Sten Anslan, Oleh Prylutskyi, Manuel Delgado-Baquerizo, Fernando T. Maestre, Jaan Pärn, Maarja Öpik, Mari Moora, Martin Zobel, Mikk Espenberg, Ülo Mander, Abdul Nasir Khalid, Adriana Corrales, Ahto Agan, Aída-M. Vasco-Palacios, Alessandro Saitta, Andrea C. Rinaldi, Annemieke Verbeken, Bobby P. Sulistyo, Boris Tamgnoue, Brendan Furneaux, Camila Duarte Ritter, Casper Nyamukondiwa, Cathy Sharp, César Marín, Daniyal Gohar, Darta Klavina, Dipon Sharmah, Dong Qin Dai, Eduardo Nouhra, Elisabeth Machteld Biersma, Elisabeth Rähn, Erin K. Cameron, Eske De Crop, Eveli Otsing, Evgeny A. Davydov, Felipe E. Albornoz, Francis Q. Brearley, Franz Buegger, Geoffrey Zahn, Gregory Bonito, Inga Hiiesalu, Isabel C. Barrio, Jacob Heilmann-Clausen, Jelena Ankuda, John Y. Kupagme, Jose G. Maciá-Vicente, Joseph Djeugap Fovo, József Geml, Juha M. Alatalo, Julieta Alvarez-Manjarrez, Kadri Põldmaa, Kadri Runnel, Kalev Adamson, Kari Anne Bråthen, Karin Pritsch, Kassim I. Tchan, Kęstutis Armolaitis, Kevin D. Hyde, Kevin K. Newsham, Kristel Panksep, Adebola A. Lateef, Liis Tiirmann, Linda Hansson, Louis J. Lamit, Malka Saba, Maria Tuomi, Marieka Gryzenhout, Marijn Bauters, Meike Piepenbring, Nalin Wijayawardene, Nourou S. Yorou, Olavi Kurina, Peter E. Mortimer, Peter Meidl, Petr Kohout, R. Henrik Nilsson, Rasmus Puusepp, Rein Drenkhan, Roberto Garibay-Orijel, Roberto Godoy, Saad Alkahtani, Saleh Rahimlou, Sergey V. Dudov, Sergei Põlme, Soumya Ghosh, Sunil Mundra, Talaat Ahmed, Tarquin Netherway, Terry W. Henkel, Tomas Roslin, Vincent Nteziryayo, Vladimir E. Fedosov, Vladimir G. Onipchenko, W. A. Erandi Yasanthika, Young Woon Lim, Nadejda A. Soudzilovskaia, Alexandre Antonelli, Urmas Kõljalg, Kessy Abarenkov
bioRxiv 2022.03.17.484796; doi: https://doi.org/10.1101/2022.03.17.484796
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Towards understanding diversity, endemicity and global change vulnerability of soil fungi
Leho Tedersoo, Vladimir Mikryukov, Alexander Zizka, Mohammad Bahram, Niloufar Hagh-Doust, Sten Anslan, Oleh Prylutskyi, Manuel Delgado-Baquerizo, Fernando T. Maestre, Jaan Pärn, Maarja Öpik, Mari Moora, Martin Zobel, Mikk Espenberg, Ülo Mander, Abdul Nasir Khalid, Adriana Corrales, Ahto Agan, Aída-M. Vasco-Palacios, Alessandro Saitta, Andrea C. Rinaldi, Annemieke Verbeken, Bobby P. Sulistyo, Boris Tamgnoue, Brendan Furneaux, Camila Duarte Ritter, Casper Nyamukondiwa, Cathy Sharp, César Marín, Daniyal Gohar, Darta Klavina, Dipon Sharmah, Dong Qin Dai, Eduardo Nouhra, Elisabeth Machteld Biersma, Elisabeth Rähn, Erin K. Cameron, Eske De Crop, Eveli Otsing, Evgeny A. Davydov, Felipe E. Albornoz, Francis Q. Brearley, Franz Buegger, Geoffrey Zahn, Gregory Bonito, Inga Hiiesalu, Isabel C. Barrio, Jacob Heilmann-Clausen, Jelena Ankuda, John Y. Kupagme, Jose G. Maciá-Vicente, Joseph Djeugap Fovo, József Geml, Juha M. Alatalo, Julieta Alvarez-Manjarrez, Kadri Põldmaa, Kadri Runnel, Kalev Adamson, Kari Anne Bråthen, Karin Pritsch, Kassim I. Tchan, Kęstutis Armolaitis, Kevin D. Hyde, Kevin K. Newsham, Kristel Panksep, Adebola A. Lateef, Liis Tiirmann, Linda Hansson, Louis J. Lamit, Malka Saba, Maria Tuomi, Marieka Gryzenhout, Marijn Bauters, Meike Piepenbring, Nalin Wijayawardene, Nourou S. Yorou, Olavi Kurina, Peter E. Mortimer, Peter Meidl, Petr Kohout, R. Henrik Nilsson, Rasmus Puusepp, Rein Drenkhan, Roberto Garibay-Orijel, Roberto Godoy, Saad Alkahtani, Saleh Rahimlou, Sergey V. Dudov, Sergei Põlme, Soumya Ghosh, Sunil Mundra, Talaat Ahmed, Tarquin Netherway, Terry W. Henkel, Tomas Roslin, Vincent Nteziryayo, Vladimir E. Fedosov, Vladimir G. Onipchenko, W. A. Erandi Yasanthika, Young Woon Lim, Nadejda A. Soudzilovskaia, Alexandre Antonelli, Urmas Kõljalg, Kessy Abarenkov
bioRxiv 2022.03.17.484796; doi: https://doi.org/10.1101/2022.03.17.484796

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