Airborne DNA reveals predictable spatial and seasonal dynamics of fungi,Nature

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Airborne DNA reveals predictable spatial and seasonal dynamics of fungi
Nature ( IF 50.5 ) Pub Date : 2024-07-10 , DOI: 10.1038/s41586-024-07658-9
Nerea Abrego _{1,

2} , Brendan Furneaux ₁ , Bess Hardwick ₂ , Panu Somervuo ₃ , Isabella Palorinne ₂ , Carlos A Aguilar-Trigueros ₁ , Nigel R Andrew _{4,

5} , Ulyana V Babiy ₆ , Tan Bao ₇ , Gisela Bazzano ₈ , Svetlana N Bondarchuk ₉ , Timothy C Bonebrake ₁₀ , Georgina L Brennan ₁₁ , Syndonia Bret-Harte ₁₂ , Claus Bässler _{13,

14,

15} , Luciano Cagnolo ₁₆ , Erin K Cameron ₁₇ , Elodie Chapurlat ₁₈ , Simon Creer ₁₉ , Luigi P D'Acqui ₂₀ , Natasha de Vere ₂₁ , Marie-Laure Desprez-Loustau ₂₂ , Michel A K Dongmo _{10,

23} , Ida B Dyrholm Jacobsen ₂₄ , Brian L Fisher _{25,

26} , Miguel Flores de Jesus ₂₇ , Gregory S Gilbert ₂₈ , Gareth W Griffith ₂₉ , Anna A Gritsuk ₉ , Andrin Gross ₃₀ , Håkan Grudd ₃₁ , Panu Halme ₁ , Rachid Hanna ₃₂ , Jannik Hansen ₃₃ , Lars Holst Hansen ₃₃ , Apollon D M T Hegbe ₃₄ , Sarah Hill ₄ , Ian D Hogg _{35,

36,

37} , Jenni Hultman _{38,

39} , Kevin D Hyde ₄₀ , Nicole A Hynson ₄₁ , Natalia Ivanova _{42,

43} , Petteri Karisto _{44,

45} , Deirdre Kerdraon ₁₈ , Anastasia Knorre _{46,

47} , Irmgard Krisai-Greilhuber ₄₈ , Juri Kurhinen ₃ , Masha Kuzmina ₄₂ , Nicolas Lecomte ₄₉ , Erin Lecomte ₄₉ , Viviana Loaiza ₅₀ , Erik Lundin ₃₁ , Alexander Meire ₃₁ , Armin Mešić ₅₁ , Otto Miettinen ₅₂ , Norman Monkhouse ₄₂ , Peter Mortimer ₅₃ , Jörg Müller _{14,

54} , R Henrik Nilsson ₅₅ , Puani Yannick C Nonti ₃₄ , Jenni Nordén ₅₆ , Björn Nordén ₅₆ , Veera Norros ₅₇ , Claudia Paz _{58,

59} , Petri Pellikka _{60,

61,

62} , Danilo Pereira _{44,

63} , Geoff Petch ₆₄ , Juha-Matti Pitkänen ₃₉ , Flavius Popa ₆₅ , Caitlin Potter ₂₉ , Jenna Purhonen _{1,

66} , Sanna Pätsi ₆₇ , Abdullah Rafiq ₁₉ , Dimby Raharinjanahary ₂₆ , Niklas Rakos ₃₁ , Achala R Rathnayaka _{40,

68} , Katrine Raundrup ₂₄ , Yury A Rebriev ₆₉ , Jouko Rikkinen _{3,

52} , Hanna M K Rogers ₁₈ , Andrey Rogovsky ₄₆ , Yuri Rozhkov ₇₀ , Kadri Runnel _{71,

72} , Annika Saarto ₆₇ , Anton Savchenko ₇₂ , Markus Schlegel ₃₀ , Niels Martin Schmidt _{33,

73} , Sebastian Seibold _{74,

75} , Carsten Skjøth _{64,

76} , Elisa Stengel ₇₇ , Svetlana V Sutyrina ₉ , Ilkka Syvänperä ₇₈ , Leho Tedersoo _{71,

79} , Jebidiah Timm ₁₂ , Laura Tipton ₈₀ , Hirokazu Toju _{81,

82} , Maria Uscka-Perzanowska ₁₈ , Michelle van der Bank ₈₃ , F Herman van der Bank ₈₃ , Bryan Vandenbrink ₃₅ , Stefano Ventura ₂₀ , Solvi R Vignisson ₈₄ , Xiaoyang Wang ₈₅ , Wolfgang W Weisser ₇₅ , Subodini N Wijesinghe _{40,

68} , S Joseph Wright ₈₆ , Chunyan Yang ₈₅ , Nourou S Yorou ₃₄ , Amanda Young ₁₂ , Douglas W Yu _{85,

87,

88} , Evgeny V Zakharov _{36,

42} , Paul D N Hebert _{36,

42} , Tomas Roslin _{3,

18} , Otso Ovaskainen _{1,

3,

89}

Affiliation

Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland.
Department of Agricultural Sciences, University of Helsinki, Helsinki, Finland.
Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
Natural History Museum, University of New England, Armidale, New South Wales, Australia.
Faculty of Science and Engineering, Southern Cross University, Northern Rivers, New South Wales, Australia.
Wrangel Island State Nature Reserve, Pevek, Russia.
Department of Biological Sciences, MacEwan University, Edmonton, Alberta, Canada.
Centro de Zoología Aplicada, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina.
Sikhote-Alin State Nature Biosphere Reserve named after K. G. Abramov, Terney, Russia.
School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China.
Institute of Marine Sciences, Consejo Superior de Investigaciones Científicas (CSIC), Passeig Marítim de la Barceloneta, Barcelona, Spain.
Institute of Arctic Biology, University of Alaska, Fairbanks, AK, USA.
Department of Conservation Biology, Institute for Ecology, Evolution and Diversity, Faculty of Biological Sciences, Goethe-University Frankfurt, Frankfurt am Main, Germany.
Bavarian Forest National Park, Grafenau, Germany.
Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth, Bayreuth, Germany.
Instituto Multidisciplinario de Biología Vegetal, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, Argentina.
Department of Environmental Science, Saint Mary's University, Halifax, Nova Scotia, Canada.
Department of Ecology, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden.
Molecular Ecology and Evolution at Bangor (MEEB), School of Biological Sciences, Bangor University, Bangor, Wales.
Research Institute on Terrestrial Ecosystems - IRET, National Research Council - CNR and National Biodiversity Future Center, Palermo, Italy.
Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
BIOGECO, INRAE, University of Bordeaux, Cestas, France.
International Institute of Tropical Agriculture (IITA), Yaoundé, Cameroon.
Greenland Institute of Natural Resources, Nuuk, Greenland.
Department of Entomology, California Academy of Sciences, San Francisco, CA, USA.
Madagascar Biodiversity Center, Parc Botanique et Zoologique de Tsimbazaza, Antananarivo, Madagascar.
Legado das Águas, Reserva Votorantin, Tapiraí, Brazil.
Department of Environmental Studies, University of California Santa Cruz, Santa Cruz, CA, USA.
Department of Life Sciences, Aberystwyth University, Aberystwyth, UK.
Biodiversity and Conservation Biology Research Unit, SwissFungi Data Center, Swiss Federal Research Institute WSL, Birmensdorf, Switzerland.
Swedish Polar Research Secretariat, Abisko Scientific Research Station, Abisko, Sweden.
Center for Tropical Research, Congo Basin Institute, University of California Los Angeles, Los Angeles, CA, USA.
Department of Ecoscience, Aarhus University, Roskilde, Denmark.
Research Unit in Tropical Mycology and Plant-Soil Fungi Interactions, Faculty of Agronomy, University of Parakou, Parakou, Republic of Benin.
Canadian High Arctic Research Station, Polar Knowledge Canada, Cambridge Bay, Nunavut, Canada.
Department of Integrative Biology, College of Biological Science, University of Guelph, Guelph, Ontario, Canada.
School of Science, University of Waikato, Hamilton, New Zealand.
Department of Microbiology, University of Helsinki, Helsinki, Finland.
Natural Resources Institute Finland (Luke), Helsinki, Finland.
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, Thailand.
Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI, USA.
Centre for Biodiversity Genomics, University of Guelph, Guelph, Ontario, Canada.
Nature Metrics North America Ltd., Guelph, Ontario, Canada.
Plant Pathology Group, Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland.
Plant Health, Natural Resources Institute Finland (Luke), Jokioinen, Finland.
Science Department, National Park Krasnoyarsk Stolby, Krasnoyarsk, Russia.
Institute of Ecology and Geography, Siberian Federal University, Krasnoyarsk, Russia.
Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.
Centre d'Études Nordiques and Canada Research Chair in Polar and Boreal Ecology, Department of Biology, Université de Moncton, Moncton, New Brunswick, Canada.
Department of Evolutionary Biology and Environmental Sciences, University of Zürich, Zurich, Switzerland.
Laboratory for Biological Diversity, Rudjer Boskovic Institute, Zagreb, Croatia.
Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland.
Centre for Mountain Futures, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China.
Department of Conservation Biology and Forest Ecology, Julius Maximilians University Würzburg, Rauhenebrach, Germany.
Department of Biological and Environmental Sciences, Gothenburg Global Biodiversity Centre, University of Gothenburg, Gothenburg, Sweden.
Norwegian Institute for Nature Research (NINA), Oslo, Norway.
Nature Solutions, Finnish Environment Institute (Syke), Helsinki, Finland.
Department of Biodiversity, Institute of Biosciences, São Paulo State University, Rio Claro, Brazil.
Department of Entomology and Acarology, Laboratory of Pathology and Microbial Control, University of São Paulo, Piracicaba, Brazil.
Department of Geosciences and Geography, Faculty of Science, University of Helsinki, Helsinki, Finland.
State Key Laboratory for Information Engineering in Surveying, Mapping and Remote Sensing, Wuhan University, Wuhan, China.
Wangari Maathai Institute for Environmental and Peace Studies, University of Nairobi, Kangemi, Kenya.
Laboratory of Biochemistry, Wageningen University, Wageningen, the Netherlands.
School of Science and the Environment, University of Worcester, Worcester, UK.
Department of Ecosystem Monitoring, Research & Conservation, Black Forest National Park, Bad Peterstal-Griesbach, Germany.
School of Resource Wisdom, University of Jyväskylä, Jyväskylä, Finland.
Biodiversity Unit, University of Turku, Turku, Finland.
School of Science, Mae Fah Luang University, Chiang Rai, Thailand.
Southern Scientific Center of the Russian Academy of Sciences, Rostov-on-Don, Russia.
State Nature Reserve Olekminsky, Olekminsk, Russia.
Mycology and Microbiology Center, University of Tartu, Tartu, Estonia.
Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia.
Arctic Research Center, Aarhus University, Roskilde, Denmark.
Forest Zoology, TUD Dresden University of Technology, Berchtesgaden, Germany.
Terrestrial Ecology Research Group, Department of Life Science Systems, School of Life Sciences, Technical University of Munich, Freising, Germany.
Department of Environmental Science, Aarhus University, Roskilde, Denmark.
Field Station Fabrikschleichach, Department of Animal Ecology and Tropical Biology (Zoology III), Julius Maximilians University Würzburg, Rauhenebrach, Germany.
Kevo Subarctic Research Institute, Biodiversity Unit, University of Turku, Utsjoki, Finland.
College of Science, King Saud University, Riyadh, Saudi Arabia.
School of Natural Science and Mathematics, Chaminade University of Honolulu, Honolulu, HI, USA.
Laboratory of Ecosystems and Coevolution, Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
Center for Living Systems Information Science (CeLiSIS), Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
African Centre for DNA Barcoding (ACDB), University of Johannesburg, Auckland Park, South Africa.
Sudurnes Science and Learning Center, Sandgerði, Iceland.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Smithsonian Tropical Research Institute, Balboa, Panama.
School of Biological Sciences, University of East Anglia, Norwich, UK.
Yunnan Key Laboratory of Biodiversity and Ecological Security of Gaoligong Mountain, Kunming Institute of Zoology, Center of Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China.
Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway.

Fungi are among the most diverse and ecologically important kingdoms in life. However, the distributional ranges of fungi remain largely unknown as do the ecological mechanisms that shape their distributions^1,2. To provide an integrated view of the spatial and seasonal dynamics of fungi, we implemented a globally distributed standardized aerial sampling of fungal spores³. The vast majority of operational taxonomic units were detected within only one climatic zone, and the spatiotemporal patterns of species richness and community composition were mostly explained by annual mean air temperature. Tropical regions hosted the highest fungal diversity except for lichenized, ericoid mycorrhizal and ectomycorrhizal fungi, which reached their peak diversity in temperate regions. The sensitivity in climatic responses was associated with phylogenetic relatedness, suggesting that large-scale distributions of some fungal groups are partially constrained by their ancestral niche. There was a strong phylogenetic signal in seasonal sensitivity, suggesting that some groups of fungi have retained their ancestral trait of sporulating for only a short period. Overall, our results show that the hyperdiverse kingdom of fungi follows globally highly predictable spatial and temporal dynamics, with seasonality in both species richness and community composition increasing with latitude. Our study reports patterns resembling those described for other major groups of organisms, thus making a major contribution to the long-standing debate on whether organisms with a microbial lifestyle follow the global biodiversity paradigms known for macroorganisms^4,5.

中文翻译：

空气中的 DNA 揭示了真菌的可预测空间和季节动态

真菌是生命中最多样化、对生态最重要的王国之一。然而，真菌的分布范围仍然很大程度上未知，影响其分布的生态机制也是如此^1,2 。为了提供真菌空间和季节动态的综合视图，我们对真菌孢子进行了全球分布的标准化空中采样³ 。绝大多数可操作的分类单元仅在一个气候区内检测到，物种丰富度和群落组成的时空模式主要由年平均气温来解释。热带地区的真菌多样性最高，但地衣真菌、环状菌根真菌和外生菌根真菌在温带地区达到了最高多样性。气候反应的敏感性与系统发育相关性相关，这表明一些真菌类群的大规模分布部分受到其祖先生态位的限制。季节性敏感性存在强烈的系统发育信号，表明某些真菌类群仅在短时间内保留了其孢子形成的祖先特征。总的来说，我们的结果表明，真菌的高度多样化王国遵循全球高度可预测的时空动态，物种丰富度和群落组成的季节性随着纬度的增加而增加。我们的研究报告的模式与其他主要生物体类群所描述的模式类似，从而为关于具有微生物生活方式的生物体是否遵循以宏观生物体闻名的全球生物多样性范式的长期争论做出了重大贡献^4,5 。

更新日期：2024-07-11

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