Soil protist life matters!
Keywords:Soil biodiversity, Microbiome, Protozoa, Soil food-web, Microfauna, Predator-prey interactions
Soils host most biodiversity on Earth, with a major fraction of its taxonomic diversity still to be uncovered and most of its functional knowledge to be determined. Much focus has been - and still is - on bacteria, fungi and animals. Clearly, without any of those components, soils would not function as they do. However, the group that constitutes the bulk of eukaryotic diversity and plays a central role for soil functioning is missing: protists. As the main consumers of the microbiome, protists shape its composition and functioning. Other less known functions performed by protists may be equally important. Protists also include primary producers, decomposers, animal parasites and plant pathogens. We briefly review the many functions protists perform in soils and argue that soil biodiversity studies that ignore protists miss some potential mechanistic insight into the drivers of observed patterns. We highlight that the immense functional repertoire of protist affects virtually every soil process, from carbon cycling to primary production, including crop production. Therefore, we call for truly integrated biodiversity assessments including protists, without which the soil food-web and processes cannot reliably be understood: protists matter!
Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch & A. Smirnov (2019): Revisions to the classification, nomenclature, and diversity of eukaryotes. – Journal of Eukaryotic Microbiology 66: 4–119.
Altenburger, A., F. Ekelund & C. S. Jacobsen (2010): Protozoa and their bacterial prey colonize sterile soil fast. – Soil Biology and Biochemistry 42: 1636–1639.
Bar-On, Y. M., R. Phillips & R. Milo (2018): The biomass distribution on Earth. – Proceedings of the National Academy of Sciences 115: 6506–6511.
Burki, F., A. J. Roger, M. W. Brown & A. G. B. Simpson (2020): The new tree of eukaryotes. – Trends in Ecology & Evolution 35:
Bonkowski, M. & M. Clarholm (2012): Stimulation of plant growth through interactions of bacteria and protozoa: testing the auxiliary microbial loop hypothesis. – Acta Protozoologica 51:
Caron, D. A., A. Z. Worden, P. D. Countway, E. Demir & K. B. Heidelberg (2008): Protists are microbes too: a perspective. – The ISME Journal 3: 4–12.
Charman, D. J. (2001): Biostratigraphic and palaeoenvironmental applications of testate amoebae. – Quaternary Science Reviews 20: 1753–1764.
de Vargas, C., S. Audic, N. Henry, J. Decelle, F. Mahe & R. Logares (2015): Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean. – Science 348: 1261605.
de Ruiter, P. C., A. M. Neutel & J. C. Moore (1995): Energetics, patterns of interaction strengths, and stability in real ecosystems. – Science 269: 1257–1260.
Decaëns, T. (2010): Macroecological patterns in soil communities. – Global Ecology and Biogeography 19: 287–302.
Delgado-Baquerizo, M., A. M. Oliverio, T. E. Brewer, A. Benavent-González, D. J. Eldridge & R. D. Bardgett (2018): A global atlas of the dominant bacteria found in soil. – Science 359:
Domonell, A., M. Brabender, F. Nitsche, M. Bonkowski & H. Arndt (2013): Community structure of cultivable protists in different grassland and forest soils of Thuringia. – Pedobiologia 56: 1–7.
Ekelund, F. (1998): Enumeration and abundance of mycophagous protozoa in soil, with special emphasis on heterotrophic flagellates. – Soil Biology and Biochemistry 30: 1343–1347.
Falkowski, P. G. (2002): The ocean’s invisible forest. – Scientific American 287: 54–61.
Fournier, B., E. Samaritani, B. Frey, C. V. W Seppey., E. Lara & T. J. Heger (2020): Higher spatial than seasonal variation in floodplain soil eukaryotic microbial communities. – Soil Biology and Biochemistry 147: 107842.
Gao, Z., I. Karlsson, S. Geisen, G. Kowalchuk & A. Jousset (2019): Protists: Puppet Masters of the Rhizosphere Microbiome. – Trends in Plant Science 24: 165–176.
Griggs, D., M. Stafford-Smith, O. Gaffney, J. Rockström, M. C. Öhman & P. Shyamsundar (2013): Sustainable development goals for people and planet. – Nature 495: 305–307.
Geisen, S. & M. Bonkowski (2018): Methodological advances to study the diversity of soil protists and their functioning in soil food webs. – Applied Soil Ecology 123: 328–333.
Geisen, S., D. H. Wall & W. H. van der Putten (2019): Challenges and opportunities for soil biodiversity in the anthropocene. – Current Biology 29: R1036–R1044.
Geisen, S., S. Hu, T. E. E. de la Cruz & G. F. Veen (in press 2020): Protists as catalyzers of microbial litter breakdown and carbon cycling at different temperature regimes. – The ISME Journal.
Geisen, S., J. Rosengarten, R. Koller, C. Mulder, T. Urich & M. Bonkowski (2015): Pack hunting by a common soil amoeba on nematodes. – Environmental Microbiology 17: 4538–4546.
Geisen, S., R. Koller, M. Hünninghaus, K. Dumack, T. Urich & M. Bonkowski (2016): The soil food web revisited: Diverse and widespread mycophagous soil protists. – Soil Biology and Biochemistry 94: 10–18.
Geisen, S., E. A. D. Mitchell, S. Adl, M. Bonkowski, M. Dunthorn, & F. Ekelund (2018): Soil protists: a fertile frontier in soil biology research. – FEMS Microbiology Reviews 42: 293–323.
Geisen, S., E. A. D. Mitchell, D. M. Wilkinson, S. Adl, M. Bonkowski & M. W. Brown (2017): Soil protistology rebooted: 30 fundamental questions to start with. – Soil Biology and Biochemistry 111: 94–103.
Geisen, S., M. J. I. Briones, H. Gan, V. M. Behan-Pelletier, V.-P. Friman & G. A. de Groot (2019): A methodological framework to embrace soil biodiversity. – Soil Biology and Biochemistry 136: 107536.
George, P. B. L., D. Lallias, S. Creer, F. M. Seaton, J. G. Kenny & R. M. Eccles (2019): Divergent national-scale trends of microbial and animal biodiversity revealed across diverse temperate soil ecosystems. – Nature Communications 10: 1107.
Glücksman, E., Bell, T., Griffiths, R. I. & Bass, D. (2010): Closely related protist strains have different grazing impacts on natural bacterial communities. – Environmental Microbiology 12: 3105–3113.
Henkes, G. J., E. Kandeler, S. Marhan, S. Scheu & M. Bonkowski (2018): Interactions of mycorrhiza and protists in the rhizosphere systemically alter microbial community composition, plant shoot-to-root ratio and within-root system nitrogen allocation. – Frontiers in Environmental Science 6: 117.
Jassey, V. E. J., C. Signarbieux, S. Hättenschwiler, L. Bragazza, A. Buttler & F. Delarue (2015): An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. – Scientific Reports 5: 16931.
Jousset, A., L. Rochat, M. Pechy-Tarr, C. Keel, S. Scheu & M. Bonkowski (2009): Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. – The ISME Journal 3: 666–674.
Kamoun, S. (2001): Nonhost resistance to Phytophthora: novel prospects for a classical problem. – Current Opinion in Plant Biology 4: 295–300.
Keeling, P. J. (2019): Combining morphology, behaviour and genomics to understand the evolution and ecology of microbial eukaryotes. – Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20190085.
Krashevska, V., D. Sandmann, M. Maraun & S. Scheu (2014): Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. – The ISME Journal 8: 1126–1134.
Krome, K., K. Rosenberg, C. Dickler, K. Kreuzer, J. Ludwig-Müller & C. Ullrich-Eberius (2010): Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. – Plant Soil 328: 191–201.
Kuikman, P. J., A. G. Jansen, J. A. van Veen & A. J. B. Zehnder (1990): Protozoan predation and the turnover of soil organic carbon and nitrogen in the presence of plants. – Biology and Fertility of Soils 10: 22–28.
Kuppardt, A., T. Fester, C. Hartig & A. Chatzinotas (2018): Rhizosphere protists change metabolite profiles in Zea mays. – Frontiers in Microbiology 9: 857.
Mahé, F., C. de Vargas, D. Bass, D., L. Czech, A. Stamatakis, E. Lara (2017): Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests. – Nature Ecology & Evolution 1: 0091.
Marcisz, K., V. E. J. Jassey, A. Kosakyan, V. Krashevska, D. J. G. Lahr & E. Lara (2020): Testate amoeba functional traits and their use in paleoecology. – Frontiers in Ecology and Evolution 8: 575966.
Nguyen, N. H., Z. Song, S. T. Bates, S. Branco, L. Tedersoo & J. Menke (2016): FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. – Fungal Ecology 20: 241–248.
Oliverio, A. M., S. Geisen, M. Delgado-Baquerizo, F. T. Maestre, B. L. Turner & N. Fierer (2020): The global-scale distributions of soil protists and their contributions to belowground systems. – Science Advances 6: eaax8787.
Orgiazzi, A., R. D. Bardgett & E. Barrios (2016): Global soil biodiversity atlas – European Commission.
Paseka, R. E., L. A. White, D. B. Van de Waal, A. T. Strauss, A. L. González & R. A. Everett (in press 2020): Disease-mediated ecosystem services: Pathogens, plants, and people. – Trends in Ecology & Evolution.
Petters, S., A. Soellinger, M. M. Bengtsson & T. Urich (2018): The soil microbial food web revisited with metatranscriptomics - predatory Myxobacteria as keystone taxon? – bioRxiv.
Phillips, H. R. P., C. A. Guerra, M. L. C. Bartz, M. J. I. Briones, G. Brown & T. W. Crowther (2019): Global distribution of earthworm diversity. – Science 366: 480.
Piwosz, K., T. Shabarova, J. Pernthaler, T. Posch, K. Šimek & P. Porcal (2020): Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. – mSphere 5: e00052–00020.
Seppey, C. V. W., D. Singer, K. Dumack, B. Fournier,
L. Belbahri & E. A. D. Mitchell (2017): Distribution patterns of soil microbial eukaryotes suggests widespread algivory by phagotrophic protists as an alternative pathway for nutrient cycling. – Soil Biology and Biochemistry 112: 68–76.
Schmidt, O., J. Dyckmans & S. Schrader (2016): Photoautotrophic microorganisms as a carbon source for temperate soil invertebrates. – Biology Letters 12: 20150646.
Schulz-Bohm, K., S. Geisen, E. R. J. Wubs, C. Song, W. de Boer & P. Garbeva (2017): The prey’s scent - Volatile organic compound mediated interactions between soil bacteria and their protist predators. – The ISME Journal 11: 817–820.
Sunagawa, S., S. G. Acinas, P. Bork, C. Bowler, S. G. Acinas & M. Babin (2020): Tara Oceans: towards global ocean ecosystems biology. – Nature Reviews Microbiology 18: 428–445.
Szelecz, I., B. Fournier, C. Seppey, J. Amendt & E. A. D.
Mitchell (2014): Can soil testate amoebae be used for estimating the time since death? A field experiment in a deciduous forest. – Forensic Science International 236: 90–98.
Tedersoo, L., M. Bahram, S. Põlme, U. Kõljalg, N. S. Yorou &
R. Wijesundera (2014): Fungal biogeography. Global diversity and geography of soil fungi. – Science 346: 1256688.
van den Hoogen, J., S. Geisen, D. Routh, H. Ferris,
W. Traunspurger & D. A. Wardle (2019): Soil nematode abundance and functional group composition at a global scale. – Nature 572: 194–198.
Wilkinson, D. M. (1998): Fragments of an entangled bank: do ecologists study most of ecology? – Oikos 82: 393–394.
Williamson, K. E., J. J. Fuhrmann, K. E. Wommack & M. Radosevich (2017): Viruses in soil ecosystems: an unknown quantity within an unexplored territory. – Annual Review of Virology 4: 201–219.
Worden, A. Z., M. J. Follows, S. J. Giovannoni, S. Wilken, A. E. Zimmerman & P. J. Keeling (2015): Environmental science. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. – Science 347: 1257594.
Xiong, W., Y. Song, K. Yang, Y. Gu, Z. Wei & G. A. Kowalchuk (2020): Rhizosphere protists are key determinants of plant health. – Microbiome 8: 27.
Zhao, Z.-B., J.-Z. He, S. Geisen, L.-L. Han, J.-T. Wang & J.-P. Shen (2019): Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. – Microbiome 7: 33.
Zhao, Z.-B., J.-Z. He, Z. Quan, C.-F. Wu, R. Sheng & L.-M. Zhang (2020): Fertilization changes soil microbiome functioning, especially phagotrophic protists. – Soil Biology and Biochemistry 148: 107863.