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      Airborne DNA reveals predictable spatial and seasonal dynamics of fungi

      research-article
      1 , 2 , , 1 , 2 , 3 , 2 , 1 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 10 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 9 , 30 , 31 , 1 , 32 , 33 , 33 , 34 , 4 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 18 , 46 , 47 , 48 , 3 , 42 , 49 , 49 , 50 , 31 , 31 , 51 , 52 , 42 , 53 , 14 , 54 , 55 , 34 , 56 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 44 , 63 , 64 , 39 , 65 , 29 , 1 , 66 , 67 , 19 , 26 , 31 , 40 , 68 , 24 , 69 , 3 , 52 , 18 , 46 , 70 , 71 , 72 , 67 , 72 , 30 , 33 , 73 , 74 , 75 , 64 , 76 , 77 , 9 , 78 , 71 , 79 , 12 , 80 , 81 , 82 , 18 , 83 , 83 , 35 , 20 , 84 , 85 , 75 , 40 , 68 , 86 , 85 , 34 , 12 , 85 , 87 , 88 , 36 , 42 , 36 , 42 , 3 , 18 , 1 , 3 , 89
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      Nature Publishing Group UK
      Biodiversity, Biogeography, Community ecology, Ecology

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          Abstract

          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 spores 3 . 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 .

          Abstract

          Using a globally distributed standardized aerial sampling of fungal spores, we 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.

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          Most cited references78

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
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            Cutadapt removes adapter sequences from high-throughput sequencing reads

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              phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data

              Background The analysis of microbial communities through DNA sequencing brings many challenges: the integration of different types of data with methods from ecology, genetics, phylogenetics, multivariate statistics, visualization and testing. With the increased breadth of experimental designs now being pursued, project-specific statistical analyses are often needed, and these analyses are often difficult (or impossible) for peer researchers to independently reproduce. The vast majority of the requisite tools for performing these analyses reproducibly are already implemented in R and its extensions (packages), but with limited support for high throughput microbiome census data. Results Here we describe a software project, phyloseq, dedicated to the object-oriented representation and analysis of microbiome census data in R. It supports importing data from a variety of common formats, as well as many analysis techniques. These include calibration, filtering, subsetting, agglomeration, multi-table comparisons, diversity analysis, parallelized Fast UniFrac, ordination methods, and production of publication-quality graphics; all in a manner that is easy to document, share, and modify. We show how to apply functions from other R packages to phyloseq-represented data, illustrating the availability of a large number of open source analysis techniques. We discuss the use of phyloseq with tools for reproducible research, a practice common in other fields but still rare in the analysis of highly parallel microbiome census data. We have made available all of the materials necessary to completely reproduce the analysis and figures included in this article, an example of best practices for reproducible research. Conclusions The phyloseq project for R is a new open-source software package, freely available on the web from both GitHub and Bioconductor.
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                Author and article information

                Contributors
                nerea.n.abrego-antia@jyu.fi
                Journal
                Nature
                Nature
                Nature
                Nature Publishing Group UK (London )
                0028-0836
                1476-4687
                10 July 2024
                10 July 2024
                2024
                : 631
                : 8022
                : 835-842
                Affiliations
                [1 ]Department of Biological and Environmental Science, University of Jyväskylä, ( https://ror.org/05n3dz165) Jyväskylä, Finland
                [2 ]Department of Agricultural Sciences, University of Helsinki, ( https://ror.org/040af2s02) Helsinki, Finland
                [3 ]Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, ( https://ror.org/040af2s02) Helsinki, Finland
                [4 ]Natural History Museum, University of New England, ( https://ror.org/04r659a56) Armidale, New South Wales Australia
                [5 ]Faculty of Science and Engineering, Southern Cross University, ( https://ror.org/001xkv632) Northern Rivers, New South Wales Australia
                [6 ]Wrangel Island State Nature Reserve, Pevek, Russia
                [7 ]GRID grid.418296.0, ISNI 0000 0004 0398 5853, Department of Biological Sciences, , MacEwan University, ; Edmonton, Alberta Canada
                [8 ]Centro de Zoología Aplicada, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, ( https://ror.org/056tb7j80) Córdoba, Argentina
                [9 ]Sikhote-Alin State Nature Biosphere Reserve named after K. G. Abramov, ( https://ror.org/002v4hw29) Terney, Russia
                [10 ]School of Biological Sciences, The University of Hong Kong, ( https://ror.org/02zhqgq86) Hong Kong SAR, China
                [11 ]Institute of Marine Sciences, Consejo Superior de Investigaciones Científicas (CSIC), ( https://ror.org/02gfc7t72) Passeig Marítim de la Barceloneta, Barcelona, Spain
                [12 ]Institute of Arctic Biology, University of Alaska, ( https://ror.org/01j7nq853) Fairbanks, AK USA
                [13 ]Department of Conservation Biology, Institute for Ecology, Evolution and Diversity, Faculty of Biological Sciences, Goethe-University Frankfurt, ( https://ror.org/04cvxnb49) Frankfurt am Main, Germany
                [14 ]Bavarian Forest National Park, ( https://ror.org/05b2t8s27) Grafenau, Germany
                [15 ]Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth, ( https://ror.org/0234wmv40) Bayreuth, Germany
                [16 ]GRID grid.423606.5, ISNI 0000 0001 1945 2152, Instituto Multidisciplinario de Biología Vegetal, , Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), ; Córdoba, Argentina
                [17 ]Department of Environmental Science, Saint Mary’s University, ( https://ror.org/010zh7098) Halifax, Nova Scotia Canada
                [18 ]Department of Ecology, Swedish University of Agricultural Sciences (SLU), ( https://ror.org/02yy8x990) Uppsala, Sweden
                [19 ]Molecular Ecology and Evolution at Bangor (MEEB), School of Biological Sciences, Bangor University, ( https://ror.org/006jb1a24) Bangor, Wales
                [20 ]GRID grid.5326.2, ISNI 0000 0001 1940 4177, Research Institute on Terrestrial Ecosystems - IRET, National Research Council - CNR and National Biodiversity Future Center, ; Palermo, Italy
                [21 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Natural History Museum of Denmark, , University of Copenhagen, ; Copenhagen, Denmark
                [22 ]GRID grid.412041.2, ISNI 0000 0001 2106 639X, BIOGECO, INRAE, , University of Bordeaux, ; Cestas, France
                [23 ]International Institute of Tropical Agriculture (IITA), ( https://ror.org/03kss9p24) Yaoundé, Cameroon
                [24 ]Greenland Institute of Natural Resources, ( https://ror.org/0342y5q78) Nuuk, Greenland
                [25 ]Department of Entomology, California Academy of Sciences, ( https://ror.org/02wb73912) San Francisco, CA USA
                [26 ]Madagascar Biodiversity Center, Parc Botanique et Zoologique de Tsimbazaza, ( https://ror.org/05fd4d895) Antananarivo, Madagascar
                [27 ]Legado das Águas, Reserva Votorantin, Tapiraí, Brazil
                [28 ]Department of Environmental Studies, University of California Santa Cruz, ( https://ror.org/03s65by71) Santa Cruz, CA USA
                [29 ]Department of Life Sciences, Aberystwyth University, ( https://ror.org/015m2p889) Aberystwyth, UK
                [30 ]GRID grid.419754.a, ISNI 0000 0001 2259 5533, Biodiversity and Conservation Biology Research Unit, SwissFungi Data Center, , Swiss Federal Research Institute WSL, ; Birmensdorf, Switzerland
                [31 ]GRID grid.417583.c, ISNI 0000 0001 1287 0220, Swedish Polar Research Secretariat, , Abisko Scientific Research Station, ; Abisko, Sweden
                [32 ]Center for Tropical Research, Congo Basin Institute, University of California Los Angeles, ( https://ror.org/046rm7j60) Los Angeles, CA USA
                [33 ]Department of Ecoscience, Aarhus University, ( https://ror.org/01aj84f44) Roskilde, Denmark
                [34 ]GRID grid.440525.2, ISNI 0000 0004 0457 5047, Research Unit in Tropical Mycology and Plant–Soil Fungi Interactions, Faculty of Agronomy, , University of Parakou, ; Parakou, Republic of Benin
                [35 ]Canadian High Arctic Research Station, Polar Knowledge Canada, ( https://ror.org/00rfash91) Cambridge Bay, Nunavut Canada
                [36 ]Department of Integrative Biology, College of Biological Science, University of Guelph, ( https://ror.org/01r7awg59) Guelph, Ontario Canada
                [37 ]School of Science, University of Waikato, ( https://ror.org/013fsnh78) Hamilton, New Zealand
                [38 ]Department of Microbiology, University of Helsinki, ( https://ror.org/040af2s02) Helsinki, Finland
                [39 ]Natural Resources Institute Finland (Luke), ( https://ror.org/02hb7bm88) Helsinki, Finland
                [40 ]Center of Excellence in Fungal Research, Mae Fah Luang University, ( https://ror.org/00mwhaw71) Chiang Rai, Thailand
                [41 ]Pacific Biosciences Research Center, University of Hawaii at Manoa, ( https://ror.org/01wspgy28) Honolulu, HI USA
                [42 ]Centre for Biodiversity Genomics, University of Guelph, ( https://ror.org/01r7awg59) Guelph, Ontario Canada
                [43 ]Nature Metrics North America Ltd., Guelph, Ontario Canada
                [44 ]Plant Pathology Group, Institute of Integrative Biology, ETH Zurich, ( https://ror.org/05a28rw58) Zurich, Switzerland
                [45 ]Plant Health, Natural Resources Institute Finland (Luke), ( https://ror.org/02hb7bm88) Jokioinen, Finland
                [46 ]Science Department, National Park Krasnoyarsk Stolby, Krasnoyarsk, Russia
                [47 ]Institute of Ecology and Geography, Siberian Federal University, ( https://ror.org/05fw97k56) Krasnoyarsk, Russia
                [48 ]Department of Botany and Biodiversity Research, University of Vienna, ( https://ror.org/03prydq77) Vienna, Austria
                [49 ]Centre d’Études Nordiques and Canada Research Chair in Polar and Boreal Ecology, Department of Biology, Université de Moncton, ( https://ror.org/029tnqt29) Moncton, New Brunswick Canada
                [50 ]Department of Evolutionary Biology and Environmental Sciences, University of Zürich, ( https://ror.org/02crff812) Zurich, Switzerland
                [51 ]Laboratory for Biological Diversity, Rudjer Boskovic Institute, ( https://ror.org/02mw21745) Zagreb, Croatia
                [52 ]GRID grid.7737.4, ISNI 0000 0004 0410 2071, Finnish Museum of Natural History, , University of Helsinki, ; Helsinki, Finland
                [53 ]GRID grid.9227.e, ISNI 0000000119573309, Centre for Mountain Futures, Kunming Institute of Botany, , Chinese Academy of Sciences, ; Kunming, China
                [54 ]Department of Conservation Biology and Forest Ecology, Julius Maximilians University Würzburg, ( https://ror.org/00fbnyb24) Rauhenebrach, Germany
                [55 ]Department of Biological and Environmental Sciences, Gothenburg Global Biodiversity Centre, University of Gothenburg, ( https://ror.org/01tm6cn81) Gothenburg, Sweden
                [56 ]Norwegian Institute for Nature Research (NINA), ( https://ror.org/04aha0598) Oslo, Norway
                [57 ]Nature Solutions, Finnish Environment Institute (Syke), ( https://ror.org/013nat269) Helsinki, Finland
                [58 ]Department of Biodiversity, Institute of Biosciences, São Paulo State University, ( https://ror.org/00987cb86) Rio Claro, Brazil
                [59 ]Department of Entomology and Acarology, Laboratory of Pathology and Microbial Control, University of São Paulo, ( https://ror.org/036rp1748) Piracicaba, Brazil
                [60 ]Department of Geosciences and Geography, Faculty of Science, University of Helsinki, ( https://ror.org/040af2s02) Helsinki, Finland
                [61 ]State Key Laboratory for Information Engineering in Surveying, Mapping and Remote Sensing, Wuhan University, ( https://ror.org/033vjfk17) Wuhan, China
                [62 ]Wangari Maathai Institute for Environmental and Peace Studies, University of Nairobi, ( https://ror.org/02y9nww90) Kangemi, Kenya
                [63 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Laboratory of Biochemistry, , Wageningen University, ; Wageningen, the Netherlands
                [64 ]School of Science and the Environment, University of Worcester, ( https://ror.org/00v6s9648) Worcester, UK
                [65 ]Department of Ecosystem Monitoring, Research & Conservation, Black Forest National Park, Bad Peterstal-Griesbach, Germany
                [66 ]School of Resource Wisdom, University of Jyväskylä, ( https://ror.org/05n3dz165) Jyväskylä, Finland
                [67 ]Biodiversity Unit, University of Turku, ( https://ror.org/05vghhr25) Turku, Finland
                [68 ]School of Science, Mae Fah Luang University, ( https://ror.org/00mwhaw71) Chiang Rai, Thailand
                [69 ]GRID grid.465325.3, ISNI 0000 0001 0042 2674, Southern Scientific Center of the Russian Academy of Sciences, ; Rostov-on-Don, Russia
                [70 ]State Nature Reserve Olekminsky, ( https://ror.org/02b47v767) Olekminsk, Russia
                [71 ]Mycology and Microbiology Center, University of Tartu, ( https://ror.org/03z77qz90) Tartu, Estonia
                [72 ]Institute of Ecology and Earth Sciences, University of Tartu, ( https://ror.org/03z77qz90) Tartu, Estonia
                [73 ]Arctic Research Center, Aarhus University, ( https://ror.org/01aj84f44) Roskilde, Denmark
                [74 ]GRID grid.4488.0, ISNI 0000 0001 2111 7257, Forest Zoology, , TUD Dresden University of Technology, ; Berchtesgaden, Germany
                [75 ]Terrestrial Ecology Research Group, Department of Life Science Systems, School of Life Sciences, Technical University of Munich, ( https://ror.org/02kkvpp62) Freising, Germany
                [76 ]Department of Environmental Science, Aarhus University, ( https://ror.org/01aj84f44) Roskilde, Denmark
                [77 ]Field Station Fabrikschleichach, Department of Animal Ecology and Tropical Biology (Zoology III), Julius Maximilians University Würzburg, ( https://ror.org/00fbnyb24) Rauhenebrach, Germany
                [78 ]Kevo Subarctic Research Institute, Biodiversity Unit, University of Turku, ( https://ror.org/05vghhr25) Utsjoki, Finland
                [79 ]College of Science, King Saud University, ( https://ror.org/02f81g417) Riyadh, Saudi Arabia
                [80 ]School of Natural Science and Mathematics, Chaminade University of Honolulu, ( https://ror.org/02xsgn598) Honolulu, HI USA
                [81 ]Laboratory of Ecosystems and Coevolution, Graduate School of Biostudies, Kyoto University, ( https://ror.org/02kpeqv85) Kyoto, Japan
                [82 ]Center for Living Systems Information Science (CeLiSIS), Graduate School of Biostudies, Kyoto University, ( https://ror.org/02kpeqv85) Kyoto, Japan
                [83 ]African Centre for DNA Barcoding (ACDB), University of Johannesburg, ( https://ror.org/04z6c2n17) Auckland Park, South Africa
                [84 ]Sudurnes Science and Learning Center, Sandgerði, Iceland
                [85 ]GRID grid.9227.e, ISNI 0000000119573309, State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, , Chinese Academy of Sciences, ; Kunming, China
                [86 ]Smithsonian Tropical Research Institute, ( https://ror.org/035jbxr46) Balboa, Panama
                [87 ]School of Biological Sciences, University of East Anglia, ( https://ror.org/026k5mg93) Norwich, UK
                [88 ]GRID grid.9227.e, ISNI 0000000119573309, 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
                [89 ]Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, ( https://ror.org/05xg72x27) Trondheim, Norway
                Author information
                http://orcid.org/0000-0001-6347-6127
                http://orcid.org/0000-0003-3522-7363
                http://orcid.org/0000-0003-3121-4047
                http://orcid.org/0000-0002-2850-2307
                http://orcid.org/0000-0002-3641-5203
                http://orcid.org/0000-0003-2045-757X
                http://orcid.org/0000-0001-5151-3947
                http://orcid.org/0000-0002-4836-1193
                http://orcid.org/0000-0003-3124-3550
                http://orcid.org/0000-0003-2387-2488
                http://orcid.org/0000-0001-9593-6925
                http://orcid.org/0000-0002-0509-5227
                http://orcid.org/0000-0003-2481-8061
                http://orcid.org/0000-0002-4653-3270
                http://orcid.org/0000-0002-5195-9903
                http://orcid.org/0000-0001-6914-3745
                http://orcid.org/0000-0002-9033-2505
                http://orcid.org/0000-0003-0635-3459
                http://orcid.org/0000-0002-3431-1785
                http://orcid.org/0000-0002-2191-0762
                http://orcid.org/0000-0001-7098-9641
                http://orcid.org/0000-0003-4807-0190
                http://orcid.org/0000-0002-8780-6044
                http://orcid.org/0000-0002-8473-5375
                http://orcid.org/0009-0005-1440-2056
                http://orcid.org/0000-0002-4479-600X
                http://orcid.org/0000-0001-7502-710X
                http://orcid.org/0000-0002-1409-1586
                http://orcid.org/0000-0002-8052-0107
                http://orcid.org/0000-0001-8894-5815
                http://orcid.org/0000-0002-2739-9774
                http://orcid.org/0000-0002-7481-0693
                http://orcid.org/0000-0002-1306-4623
                http://orcid.org/0000-0002-5268-5799
                http://orcid.org/0000-0001-8498-2715
                http://orcid.org/0000-0002-2110-3709
                http://orcid.org/0000-0001-5156-8593
                http://orcid.org/0000-0002-7308-3623
                http://orcid.org/0000-0002-4166-6218
                http://orcid.org/0000-0002-7968-4489
                http://orcid.org/0000-0001-5992-9568
                http://orcid.org/0000-0002-1635-1249
                http://orcid.org/0000-0002-5118-2671
                http://orcid.org/0000-0002-3362-3285
                http://orcid.org/0000-0002-8234-8195
                http://orcid.org/0000-0002-8134-3675
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                http://orcid.org/0000-0001-9750-4421
                Article
                7658
                10.1038/s41586-024-07658-9
                11269176
                38987593
                8b91018f-6d20-4b21-959a-40a17aa12ff4
                © The Author(s) 2024

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                : 3 January 2024
                : 4 June 2024
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