Ecosystem type drives soil eukaryotic diversity and composition in Europe

Soil eukaryotes play a crucial role in maintaining ecosystem functions and services, yet the factors driving their diversity and distribution remain poorly understood. While many studies focus on some eukaryotic groups (mostly fungi), they are limited in their spatial scale. Here, we analyzed an unprecedented amount of observational data of soil eukaryomes at continental scale (787 sites across Europe) to gain further insights into the impact of a wide range of environmental conditions (climatic and edaphic) on their community composition and structure. We found that the diversity of fungi, protists, rotifers, tardigrades, nematodes, arthropods, and annelids was predominantly shaped by ecosystem type (annual and permanent croplands, managed and unmanaged grasslands, coniferous and broadleaved woodlands), and higher diversity of fungi, protists, nematodes, arthropods, and annelids was observed in croplands than in less intensively managed systems, such as coniferous and broadleaved woodlands. Also in croplands, we found more specialized eukaryotes, while the composition between croplands was more homogeneous compared to the composition of other ecosystems. The observed high proportion of overlapping taxa between ecosystems also indicates that DNA has accumulated from previous land uses, hence mimicking the land transformations occurring in Europe in the last decades. This strong ecosystem-type influence was linked to soil properties, and particularly, soil pH was driving the richness of fungi, rotifers, and annelids, while plant-available phosphorus drove the richness of protists, tardigrades, and nematodes. Furthermore, the soil organic carbon to total nitrogen ratio crucially explained the richness of fungi, protists, nematodes, and arthropods, possibly linked to decades of agricultural inputs. Our results highlighted the importance of long-term environmental variables rather than variables measured at the time of the sampling in shaping soil eukaryotic communities, which reinforces the need to include those variables in addition to ecosystem type in future monitoring programs and conservation efforts.

[1]  C. Ballabio,et al.  LUCAS Soil Biodiversity and LUCAS Soil Pesticides, new tools for research and policy development , 2022, European Journal of Soil Science.

[2]  Hongbo He,et al.  Manure application accumulates more nitrogen in paddy soils than rice straw but less from fungal necromass , 2021 .

[3]  Heidi K. Mod,et al.  Comparative analysis of diversity and environmental niches of soil bacterial, archaeal, fungal and protist communities reveal niche divergences along environmental gradients in the Alps , 2021, Soil Biology and Biochemistry.

[4]  A. Heintz‐Buschart,et al.  Large‐scale drivers of relationships between soil microbial properties and organic carbon across Europe , 2021, Global Ecology and Biogeography.

[5]  G. Kowalchuk,et al.  A global overview of the trophic structure within microbiomes across ecosystems. , 2021, Environment international.

[6]  L. Tedersoo,et al.  Towards revealing the global diversity and community assembly of soil eukaryotes. , 2021, Ecology letters.

[7]  D. Bass,et al.  Protist taxonomic and functional diversity in soil, freshwater and marine ecosystems. , 2020, Environment international.

[8]  P. Karlovsky,et al.  Improved normalization of species count data in ecology by scaling with ranked subsampling (SRS): application to microbial communities , 2020, PeerJ.

[9]  T. Heger,et al.  Higher spatial than seasonal variation in floodplain soil eukaryotic microbial communities , 2020, Soil Biology and Biochemistry.

[10]  Benjamin L Turner,et al.  The global-scale distributions of soil protists and their contributions to belowground systems , 2020, Science Advances.

[11]  C. Guerra,et al.  Towards an integrative understanding of soil biodiversity , 2019, Biological reviews of the Cambridge Philosophical Society.

[12]  Y. Kuzyakov,et al.  Manure over crop residues increases soil organic matter but decreases microbial necromass relative contribution in upland Ultisols: Results of a 27-year field experiment , 2019, Soil Biology and Biochemistry.

[13]  D. Schneider,et al.  Changes in Trophic Groups of Protists With Conversion of Rainforest Into Rubber and Oil Palm Plantations , 2019, Front. Microbiol..

[14]  E. Cooper,et al.  Dead or Alive; or Does It Really Matter? Level of Congruency Between Trophic Modes in Total and Active Fungal Communities in High Arctic Soil , 2019, Front. Microbiol..

[15]  R. H. Nilsson,et al.  Locality or habitat? Exploring predictors of biodiversity in Amazonia , 2018, Ecography.

[16]  H. Tuomisto,et al.  High-throughput metabarcoding reveals the effect of physicochemical soil properties on soil and litter biodiversity and community turnover across Amazonia , 2018, PeerJ.

[17]  C. Ballabio,et al.  LUCAS Soil, the largest expandable soil dataset for Europe: a review , 2018 .

[18]  Stephen E. Fick,et al.  WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas , 2017 .

[19]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[20]  Panos Panagos,et al.  Reply to “The new assessment of soil loss by water erosion in Europe. Panagos P. et al., 2015 Environ. Sci. Policy 54, 438–447—A response” by Evans and Boardman [Environ. Sci. Policy 58, 11–15] , 2016 .

[21]  N. Fierer,et al.  Relic DNA is abundant in soil and obscures estimates of soil microbial diversity , 2016, Nature Microbiology.

[22]  J. Frouz,et al.  Intensive agriculture reduces soil biodiversity across Europe , 2015, Global change biology.

[23]  T. Wubet,et al.  Effects of long‐term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach , 2014, Molecular ecology.

[24]  Pelin Yilmaz,et al.  The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks , 2013, Nucleic Acids Res..

[25]  Scott T. Bates,et al.  Global biogeography of highly diverse protistan communities in soil , 2012, The ISME Journal.

[26]  Edward Ayres,et al.  Molecular study of worldwide distribution and diversity of soil animals , 2011, Proceedings of the National Academy of Sciences.

[27]  J. Kaplan,et al.  The prehistoric and preindustrial deforestation of Europe , 2009 .

[28]  Budiman Minasny,et al.  A conditioned Latin hypercube method for sampling in the presence of ancillary information , 2006, Comput. Geosci..

[29]  P. Krogh,et al.  Comparing earthworm biodiversity estimated by DNA metabarcoding and morphology-based approaches , 2023, Applied Soil Ecology.

[30]  Martha B. Dunbar,et al.  Soil biodiversity and DNA barcodes: opportunities and challenges , 2015 .

[31]  R. Neilson,et al.  Determination of the optimal soil sample size to accurately characterise nematode communities in soil , 2015 .

[32]  S. Salzberg,et al.  FLASH: fast length adjustment of short reads to improve genome assemblies , 2011, Bioinform..