Enhancing Soil Biodiversity
Soil: the final frontier. At NIOO, we are on a mission to explore the strange world beneath our feet, to seek out new soil-borne life, uncover new miniature civilisations, and to boldly take humankind where it could not go before. New technologies have taught us more about the earth’s vast oceans and deep space than we know about the life directly below our feet. This we need to change.
We know the soil is a bizarre place, filled with life but empty at the same time. Its 3D structure is hugely complex and provides habitat for thousands of species per gram of soil. Local pockets of food drive abundances up to astronomical numbers, but in between these oases lie vast, interstellar spaces without much life at all.
Together, these life forms – often alien to us – are responsible for soil fertility, storing more carbon (~1200 Gt) than all trees together1, and providing clean drinking water for human communities. They also help to maintain the diversity of plants and animals aboveground. Overall, their actions represent a monetary value of 5–9 times the world’s GDP, and that’s not even counting their human health benefits.
Who are they? Where do they come from? What do they do? How can they help sustain humanity in the long run? These are the big questions we face. Welcome to the real terra incognita!
Who are these belowground aliens?
What do they do?
What do they do for us?
What threatens soil biodiversity?
How can we live better with the biodiversity belowground?
Who are these belowground aliens ?
You will likely know that bacteria, fungi and earthworms live in soil, but it may come as a surprise that the number of bacteria in a single gram of soil (4–20 x 109) exceeds the number of humans on earth2. It does not stop there: a gram of soil may contain 100 metres of fungal hyphae and thousands of bacterial and protist species. Compared to oceans and animals’ bodies, the microbial diversity in the soil – and particularly in the plant rhizosphere – is dazzling3.
Soil organisms represent as much as 25% of the 1.5 million described living species, but science probably knows less than 10% of the species living belowground4. Tardigrades, the famous ‘water bears’, are some of the most resilient organisms we know: their ability to desiccate completely allows them to survive even in outer space5. Yet we don’t even know how many tardigrades there are in soil! Furthermore, the soil is inhabited by a menagerie of smaller and larger fauna, including nematodes, pot worms, springtails, mites and the more familiar millipedes, wood lice, ants, termites, earthworms, voles and moles.
However, the smallest and most mysterious of the soil’s inhabitants are viruses, and we even don’t know if they are really alive. Yet these nanoscale (30–80 nm) undead legions (up to 1010 virus particles per gram of soil) may be responsible for the deaths of most bacteria in soil, and potentially other organisms too6.
What do they do ?
The same as you, actually: just living their lives. Trying not to be put out of a job while making a better life for their significant others. Microbes as well as the larger soil fauna all forage for food within the complex soil matrix7, they grow or rest if conditions are adverse8, they make love, procreate and – at times – go to war.
Bacteria and fungi do a lot of the heavy lifting in soils. They decompose dead organic material, i.e. leaves, roots, animal poop and carcasses, but they are constantly being hunted by giant worms (nematodes), unicellular misfits (protozoa), and the legions of the undead (viruses). Nematodes – giants by comparison (up to 2 mm) – move through the soil like large vacuum cleaners, sucking up microbes as they move around. Even the tiny single-celled protozoa (less than 0.16 mm), amoebas, ciliates and flagellates, seek out their bacterial prey, which they do by smelling the scent of specific species (using the specific palette of volatile organic compounds emitted by the bacteria)9.
Like fish, the larger soil organisms generally eat the smaller ones: amoebas eat bacteria, nematodes eat amoebas and the carnivorous mites – the lions of the soil – eat almost everything7. But it is not always like that. Some fungi are known to trap and consume nematodes, others specialise in feeding on ground-dwelling insects. Indeed, the tiny protozoa have been observed to hunt together in packs, killing a mammoth-sized nematode in the process10: the small eating the big! Our understanding of the organisation of the soil food web is still evolving.
Many soil organisms fall on hard times at some point in their lives and go into a dormant resting state to survive. Many bacteria and fungi hibernate - using e.g. spores, conidia, cysts, dwarf cells - and can live like that for decades or centuries (and some even longer)8. In fact, because life belowground is hard, most microbes (~80% of cells) are dormant at any one time. Earthworms coil up into diapause, taking a break when the soil is too dry, which allows them to cope with summer droughts. And of course, among soil animals our favourite tardigrades can survive in hibernation (actually cryptobiosis, a superpower they derive from a combination of encystment, anoxybiosis, cryobiosis, osmobiosis, and anhydrobiosis) for decades7, much longer than aboveground bears.
Microbes can deploy a range of chemical weapons to subdue their competitors, releasing antimicrobial compounds into the soil matrix for instance, where bacteria and fungi in particular strive for dominance11. While predation and chemical warfare among soil organisms are often recorded, soil organisms cooperate as well. Classic symbioses of plant roots with Rhizobia (N2-fixers) and mycorrhizal fungi are well known, although even these friends can turn on their hosts12.
Recent discoveries have highlighted that many microbes cannot survive on their own. Many have lost the metabolic pathways needed to synthesize all the necessary amino acids, vitamins, nucleotides and growth factors and regularly exchange these with other organisms: both other microbes and larger organisms such as animals, protozoa and plants13,14. In fact, certain bacteria develop specialised networks of nanotubes that physically connect very different bacterial species for the exchange of essential amino acids15. It’s a division of metabolic labour16.
What do they do for us ?
The soil food web, the brown mirror of the green food web aboveground, is responsible for the recycling and upcycling of organic matter. Microbes decompose leaves, roots, animal poop and carcasses and run your compost heap. In the process they release important nutrients that are needed for plant growth (e.g. in the form of amino acids or inorganic nitrogen17). Other microbes release acids and enzymes into the soil, allowing them to obtain nutrients from sheer rock!
And that’s not all. The microbes truly transform the organic matter, stabilising carbon (and other elements such as nitrogen) in the soil in the long term by gluing it onto mineral soil particles. This gluing is important, as it also sticks together the mineral particles to form aggregates and thus creates soil structure so that the soil can remain stable despite erosion by wind and water. The mineral-associated carbon and the aggregates also strongly increase the soil’s ability to act as a sponge. This is important for the soil’s capacity to store and retain water18. In addition to storing carbon, several soil microbiota can consume methane and nitrous oxide – both potent greenhouse gases – and reduce emissions into the atmosphere. Together, these ecosystem services represent an estimated monetary value of 5–9 times the world’s GDP! (For these numbers we extrapolated The Nature Conservancy’s estimate by rescaling the US value by arable land area).
This is without taking into account soil biodiversity’s role in human health. Human, animal and ecosystem health are strongly connected through food, air, water and animal-mediated diseases (e.g. zoonoses): interconnections understood under the term One Health. Many soil microorganisms travel through the air to disperse – their small-sized spores allow them to surf the air waves for thousands of kilometres19 – and air samples include many potential plant and animal pathogens20. Poor land management and climate change can undermine the soil’s ‘immune responses’21 and increase the numbers of soil-borne pests and diseases, but can also weaken human health by lowering food quality22. On the other hand, exposure to soil organisms – e.g. in parks and playgrounds – helps to lessen allergies by building tolerance in children. Soil biodiversity likely also harbours some of the key therapeutics (antibiotics, medicines) of the future.
What threatens soil biodiversity ?
Despite the huge value of soil biodiversity for aboveground nature and human health and wellbeing, many soil organisms are under threat. Mushrooms, the reproductive parts of important soil fungi, have declined by 45% over the last century23, soil microbial communities are becoming more alike across the globe24 – implying a huge net loss in soil biodiversity – and half of all soil biodiversity hotspots area at risk, as they do not correspond to aboveground biodiversity hotspots25.
A range of human actions and changes to the environment negatively affect soil biodiversity. This includes deforestation and agricultural intensification – e.g. tillage27 – together driving losses in soil organic matter and mechanically disturbing soil and fungi hyphae. But it also includes salinisation, soil erosion, soil sealing and compaction, acidification, climate change, and invasive species. We need to learn how to work better with the diversity belowground to enable the sustainable use of land.
How can we live better with the biodiversity belowground ?
At NIOO, the sustainable use of land (and water) is a central research theme. For soil biodiversity, we have launched the Netherlands Soil Ecology and Biodiversity Centre (‘IJkcentrum voor de Bodem’ in Dutch). Here, we bring together data and knowledge on the state of, and trends in, soil biodiversity and how it can be steered for optimal soil functioning at a national level.
We analyse big soil biodiversity data with AI to predict how soil multifunctionality can be optimised. We survey soil biodiversity in thousands of samples according to a representative sampling design across the Netherlands, studying abundance and diversity from bacteria to earthworms in all major land use types using modern high-throughput techniques. We link this to data on the local environment, management and soil functioning using standardised methods. Next, we test how we can steer soil biodiversity for soil multifunctionality, for instance in the Soil Ecotrons: a large experimental facility at NIOO, where we manipulate soil and plant diversity to study how we can transition intensively used agricultural soils to sustainable use.
Using this knowledge, we can effectively steer soil biodiversity. Through soil inoculation28 for instance, which has proved successful at improving nature restoration29 and which may help make our forests future-proof and can also improve crop health.
We investigate how we can close material cycles for sustainable production and consumption, and look at alternative plant production systems and how we can minimise greenhouse gas emissions from soils. We coordinate the national Soil Animal Days, a citizen science project to assess the state of, and trends in, soil biodiversity at schoolyards, parks and people’s own backyards involving thousands of volunteer citizen scientists each year. Internationally, we are a contributor to the FAO-led global state of knowledge report on soil biodiversity, have helped create the EU research agenda and are a founding member of the Global Soil Biodiversity Initiative.
At NIOO, we study how we can 'forewild –'the forward-looking version of rewilding – our soils so that we can safeguard (agro)ecosystem functioning now and in the future.
1. Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3, 909–912 (2013).
2. Bardgett, R. D. & Van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).
3. Thompson, L. R. et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551, 457–463 (2017).
4. Decaëns, T. Macroecological patterns in soil communities. Glob. Ecol. Biogeogr. 19, 287–302 (2010).
5. Jönsson, K. I., Rabbow, E., Schill, R. O., Harms-Ringdahl, M. & Rettberg, P. Tardigrades survive exposure to space in low Earth orbit. Curr. Biol. 18, R729–R731 (2008).
6. Kuzyakov, Y. & Mason-Jones, K. Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions. Soil Biol. Biochem. 127, 305–317 (2018).
7. Coleman, D. C., Callaham, M. A. & Crossley, D. A. Fundamentals of Soil Ecology (third edition). (Academic Press, Elsevier Inc., 2018).
8. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).
9. Schulz-Bohm, K. et al. The prey’s scent – Volatile organic compound mediated interactions between soil bacteria and their protist predators. ISME J. 11, 817–820 (2017).
10. Geisen, S. et al. Pack hunting by a common soil amoeba on nematodes. Environ. Microbiol. 17, 4538–4546 (2015).
11. Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).
12. Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407 (2010).
13. D’Souza, G. et al. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat. Prod. Rep. 35, 455–488 (2018).
14. D’Souza, G. et al. Less Is More: Selective Advantages Can Explain the Prevalent Loss of Biosynthetic Genes in Bacteria. Evolution 68, 2559–2570 (2014).
15. Pande, S. et al. Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat. Commun. 6, 6238 (2015).
16. Pande, S. et al. Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J. 8, 953–962 (2014).
17. Schimel, J. P. & Bennett, J. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602 (2004).
18. Lal, R. Soil organic matter and water retention. Agron. J. 112, 3265–3277 (2020).
19. Meola, M., Lazzaro, A. & Zeyer, J. Bacterial Composition and Survival on Sahara Dust Particles Transported to the European Alps. Front. Microbiol. 6, art1454 (2015).
20. De Groot, G. A. et al. The aerobiome uncovered: multi-marker metabarcoding reveals potential drivers of turn-over in the full microbial community in the air. Environ. Int. 154, 106551 (2021).
21. Raaijmakers, J. M. & Mazzola, M. Soil immune responses. Science 352, 1392–1393 (2016).
22. Wall, D. H., Nielsen, U. N. & Six, J. Soil biodiversity and human health. Nature 528, 69–76 (2015).
23. Averill, C. et al. Defending Earth’s terrestrial microbiome. Nat. Microbiol. 1–9 (2022) doi:10.1038/s41564-022-01228-3.
24. Guerra, C. A. et al. Global projections of the soil microbiome in the Anthropocene. Glob. Ecol. Biogeogr. 30, 987–999 (2021).
25. Cameron, E. K. et al. Global mismatches in aboveground and belowground biodiversity. Conserv. Biol. 33, 1187–1192 (2019).
26. FAO, ITPS, GSBI, SCBD, & EC. State of knowledge of soil biodiversity - Status, challenges and potentialities: Report 2020. (FAO, 2020). doi:10.4060/cb1928en.
27. Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985 (2015).
28. Wubs, E. R. J., Van der Putten, W. H., Bosch, M. & Bezemer, T. M. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2, 16107 (2016).
29. Gerrits, G. M. et al. Synthesis on the effectiveness of soil translocation for plant community restoration. J. Appl. Ecol. (2023) doi:10.1111/1365-2664.14364.