Plant-soil interactions: the cycle of life

Last spring, I gave a TED talk about plant-soil interactions and their importance in the global carbon cycle at a TEDx event organised by Amsterdam University College. You can watch the video below, but for those of you who rather read (actually, I am one of those people, as I never have the patience to watch a video from beginning to end!) you can also read the full text below.

Do you ever think about soils? Do you ever think about soils, other than, when your boots are muddy, or your vegetables dirty? Well, I’m going to talk about soils.

Soils! Without soils, we would not be here. Soils sustain all life on land. And that is because all energy flows through soils, via photosynthesis and respiration.

Have soils always been here?

No!

Have you ever thought about how soils are formed? Where plants came from? And the tiny invisible microbes that live in the soil?

More than 4.5 billion years ago, there was no soil. There wasn’t even life. There were only oceans. But somewhere between 4.5 and 3.5 billion years ago, the first microorganisms appeared in the oceans. There wasn’t even free oxygen at that time! But then, photosynthesis evolved in bacteria, and cyanobacteria started producing oxygen around 2.7 billion years ago. About 1.5 billion years ago, the first fungi appeared, and much later, around 500 million years ago, the first land plants arose. Probably, photosynthesis in these plants was derived from photosynthetic bacteria inside plant cells (the endosymbiosis theory). Those first land plants – like this little liverwort – had no, or very rudimentary roots (remember, there was no soil that they could grow their root in, only rock!), and were likely helped on land by symbiotic fungi. 

And this is where soil started to form. 

A photo of a soil profile, showing distinct layers, with vegetation and a dark organic layer at the top, and bedrock at the bottom
A soil profile. Photo: Richard Bardgett.

Plants started to draw down CO2 from a very high CO2 atmosphere. In those times, CO2 concentrations in the atmosphere were more than 1000 ppm – that means that out of one million molecules in the air, one thousand are CO2 molecules – and maybe even as high as 4000 ppm – compare that to our current atmospheric CO2levels of 400 ppm! In exchange for this carbon (that’s the C in CO2), mycorrhizal fungi provided the plants with nutrients. Organic matter, in the form of plant, and also fungal tissue, accumulated, and plants and fungi also enhanced mineral weathering through the secretion of organic acids. This process of soil formation drew down even more CO2 from the air. And then, CO2 levels started to drop.

Let that drop. It’s likely – this is a theory, because it’s very hard to look into the past and make causal inferences – that plants and fungi caused a decline in CO2 levels from 4000 ppm at the start of the Palaeozoic – that’s about 500 million years ago – to around 400 ppm at the end of the Palaeozoic 200 million years later.

Right. So, but, OK, I said I was going to talk about a cycle. The cycle, or circle, of life. And this process that I’ve just described is a one-way process, right? Like a dead-end road. Plants and symbiotic fungi take up CO2, stimulate weathering, and bury that CO2 through forming soils. But if that was the *only* process, the soil would just be piling up carbon, and the atmosphere would become deprived of CO2. And as all of you know, that certainly isn’t happening.

There’s one process I’ve been ignoring in what I just told you.

And that’s: heterotrophy, or, decomposition. Many organisms derive their energy from decomposing or eating, organic substrates, like dead plant or microbial tissue. And this strategy evolved long before land plants! Decomposing organisms, initially only bacteria and other single-celled organisms, later also critters like arthropods, and much later, also US! – we all use energy and carbon for growth and metabolism, but, importantly, in doing so, we release part of that carbon back into the atmosphere as CO2. That’s respiration. 

How I see the circle of life in my mind. Plants photosynthesise and take up CO2 from the atmosphere. Part of this carbon is allocated below ground, via roots and their exudates, and decomposed by soil organisms. As a result, CO2 is emitted back into the atmosphere, but a small part of that carbon is locked up in the soil for a long time.

So there we have our cycle. And in fact, this cycle consists of more cycles.

Plants use the energy of sunlight to generate glucose from CO2, and the energy is captured in the chemical bonds in glucose, in the Calvin cycle.

Heterotrophic organisms in the soil can subsequently use that energy by breaking down these bonds in glucose in the Krebs cycle, which generates energy and releases CO2. But they do something else, too. When decomposing organic material in the soil, they release nutrients from that material, thus sustaining plant growth!

Can you imagine a world without these soil organisms? No dead plant material would be decomposed. It would just pile up. No nutrients would be released for plants to continue growing, so plant growth would stop, and the world would turn brown. We wouldn’t be able to grow crops. There would be no grazers anymore, no birds that feed on seeds, no pollinators that need flowers. The world as we know it would grind to a halt. This is how important soil organisms are!

Now I’ve only been talking about “plants”, “fungi”, “microbes”, ignoring the vast diversity within these groups of organisms! For plants, most people obviously know how diverse they are– we can see them! But for soil fungi and bacteria? We can’t. And as we say in Dutch: unknown makes unloved. 

Soils harbour at least 25% of all biodiversity on Earth! In one handful of soil, we can find millions of bacterial cells of thousands of different species, and hundreds of metres of fungal hyphae! There are approximately four and a half times 10 to the power 20 (that’s 4.5 plus 19 zeros) nematodes living in the upper layer of global soils– that is around one hundred billion nematodes per human being, with a total biomass that is around 80% of the biomass of all humans!  Yet, we tend to ignore this vast biodiversity, and we don’t think about how these organisms rule the world. We don’t think about the intricate networks they form and their interactions – connections! – with plants – the result of billions of years of evolution, but under threat now by land-use change and climate change.

Now, as a result of billions of years of growth of plants, soil organisms, animals on land (and algae and plankton in the oceans), the continuous burial of these organic compounds and their subjection to heat and pressure turned these materials into fossil fuels. Fossil fuels that we are now rapidly burning, and by doing so, we are releasing the CO2 back into the atmosphere that has been locked inside these ancient remains for millions of years. 

Now, you might think: plants and soil organisms have managed to bring down CO2 levels before – why can’t they do this again?

Well, the circumstances are rather different. Back then, we had no plants, no soils, and very little biomass, so just the appearance of these had immense potential to draw down CO2. Now, we have a vegetated planet with developed and sometimes highly weathered soils. So the ADDITIONAL CO2 drawdown is going to be much more limited. But more importantly, drawing down this CO2 took a LONG time – around 200 million years. 

Moreover, we are disrupting the plant-microbial interactions that are so crucial for this drawdown. We are disrupting them through the destruction of habitats. We are disrupting them by ploughing up the soil. We are disrupting them by growing plants in places where they would normally not grow. We are disrupting them through ferrying species around the world, introducing novel, alien species to places where they don’t have their natural enemies present in the soil, and where they can, as a consequence, take over. But we are also disrupting them through human-induced climate change. This climate change is happening so rapidly that evolutionary mechanisms of adaptation between plants and microbes can likely not keep up.

So while many people think that elevated CO2 levels will result in more plant growth, more ecosystem uptake of CO2, and more carbon locked up in the soil, the reality is that there are many constraints on this process. Not only are there constraints on land use – we simply cannot use all land to optimise ecosystem uptake of CO2 because that would mean we would be planting forests at the expense of valuable, biodiverse, or protected ecosystems that can store less carbon – but in many places not CO2 is the limiting factor for plant growth, but the presence of water and nutrients to support this plant growth. Moreover, climate change itself is already affecting the capacity of plants and microbes to work together in taking up this CO2.

We don’t often think about this. When we think about the impact of climate change, we think about the trees in the Amazon rainforest taking up less CO2, and we think about the permafrost soils thawing and releasing CO2. We rarely think about the interactions between plants and microbes that govern the carbon cycle. Yet it is those interactions that are crucial for the functioning of ecosystems and the response to climate change.

Increasing temperatures can improve plant growth in some regions, potentially drawing down more CO2, but they also increase soil – heterotrophic – respiration and the release of previously locked up CO2 into the atmosphere. But more frequent extreme weather events also affect plant growth and soil microbial communities. Droughts can result in big peaks of CO2 loss into the atmosphere when soils are rewetted. And because plants are better able to cope with these extreme events when they are growing with their own soil microbes, we have unknowingly already compromised the capacity of our ecosystems to cope with these extreme events, and we risk these ecosystems becoming a source of CO2 instead of drawing down CO2.

OK. So you might notice that I can talk about this, without batting an eyelid. I can talk about this, because this is my study system, and I can look at it technically, and curiously. I am a scientist that wants to understand these responses, and the role that plant-microbe integrations play in them. I can professionally distance myself, yet still be in awe of these beautiful organisms and their interactions. But when I take one step back, and I talk about what this actually means to friends and family, and I look at my children, and I picture the world in 30 years’ time? That’s when it gets me.

But there is hope! There are things that we can do to make sure our soils do not lose their carbon, and to make sure we foster the capacity of plants and soils to take up CO2

We need to protect and restore ecosystems. We need to stay clear of unthinkingly planting forests everywhere! If not planted in the right place, doing this will only disrupt plant-soil interactions and may even lead to a loss of soil carbon! 

We need to map and understand the distribution of soil biodiversity, and have specific conservation guidelines for restoring and protecting this vast reservoir of biodiversity of which most species have not even been discovered and described yet.

We need to protect the diversity and the genetic diversity of plant species, because that reservoir of biodiversity may help us adapt crop plants to a different climate. 

We need a fundamental understanding of the communication, the ecological and evolutionary mechanisms, of plant-microbe interactions. Only if we have that understanding, we will be able to understand the significance of these interactions in the functioning of our ecosystems, and truly use that knowledge for restoring ecosystems, and making our food production systems more sustainable. 

We need to let the plants and the microbes do their work. 

And for that, we need to STOP. BURNING. FOSSIL. FUELS. 

Sources used

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de Vries, F. T., R. I. Griffiths, C. G. Knight, O. Nicolitch and A. Williams (2020). “Harnessing rhizosphere microbiomes for drought-resilient crop production.” Science 368 (6488): 270-274.

de Vries, F. T., A. Williams, F. Stringer, R. Willcocks, R. McEwing, H. Langridge and A. L. Straathof (2019). “Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling.” New Phytologist 224 (1): 132-145.

FAO, ITPS, GSBI, SCBD and EC (2020). State of knowledge of soil biodiversity – Status, challenges and potentialities. Rome.

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van den Hoogen, J., S. Geisen, D. Routh, H. Ferris, W. Traunspurger, D. A. Wardle, R. G. M. de Goede, B. J. Adams, W. Ahmad, W. S. Andriuzzi, R. D. Bardgett, M. Bonkowski, R. Campos-Herrera, J. E. Cares, T. Caruso, L. de Brito Caixeta, X. Chen, S. R. Costa, R. Creamer, J. Mauro da Cunha Castro, M. Dam, D. Djigal, M. Escuer, B. S. Griffiths, C. Gutiérrez, K. Hohberg, D. Kalinkina, P. Kardol, A. Kergunteuil, G. Korthals, V. Krashevska, A. A. Kudrin, Q. Li, W. Liang, M. Magilton, M. Marais, J. A. R. Martín, E. Matveeva, E. H. Mayad, C. Mulder, P. Mullin, R. Neilson, T. A. D. Nguyen, U. N. Nielsen, H. Okada, J. E. P. Rius, K. Pan, V. Peneva, L. Pellissier, J. Carlos Pereira da Silva, C. Pitteloud, T. O. Powers, K. Powers, C. W. Quist, S. Rasmann, S. S. Moreno, S. Scheu, H. Setälä, A. Sushchuk, A. V. Tiunov, J. Trap, W. van der Putten, M. Vestergård, C. Villenave, L. Waeyenberge, D. H. Wall, R. Wilschut, D. G. Wright, J.-i. Yang and T. W. Crowther (2019). “Soil nematode abundance and functional group composition at a global scale.” Nature 572 (7768): 194-198.

And also a lot of work in progress from my group!

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