Body Extravagant

Melvin Sheldrake and Florian Walder

A Conversation between Merlin Sheldrake and Florian Walder about fungal networks. Merlin is a London based scientist and author of Entangled Life: How Fungi Make Our Worlds, Change Our Minds, and Shape Our Futures. Florian is a scientist at Agroscope in Zürich and works on the role of soil microbes in agriculture.

I wanted to start by discussing mycoheterotrophic plants. I like mycoheterotrophic plants because they show an extreme example of resource exchange between plants and fungi in mycorrhizal symbiosis - underlining that mycorrhizal associations does not only comprise strictly mutual exchange.

I agree, and find it very helpful to think of the symbiotic continuum between parasitism at one extreme, where one partner benefits at the expense of another, and mutualism at the other extreme, where both partners benefit. In reality, most relationships will be sliding around somewhere on this spectrum. Mycoheterotrophs are really helpful for thinking about the mycorrhizal association in general because they seem to take without giving anything in return - at least the full mycoheterotrophs that have lost the ability to photosynthesise. They demonstrate that the ancient relationship between plants and fungi, which is often very intricately managed, can be very one-sided. So, yes, I think they're really important cases. And of course, there are lots to be a mycoheterotroph – the lifestyle has evolved over 40 times independently. Some plants, like many orchids, receive nutrients and carbon from the fungus when they’re young, and start paying back into the fungal network when they get older and start photosynthesizing. But then there's also really interesting examples, in ferns (in genera including Ophioglossum and Lycopodium). These plants have two stages of their lifecycle – a ‘juvenile’ gametophyte stage, which doesn’t photosynthesise, and an ‘adult’ sporophyte stage which does. Gametophytes are small underground structures that don’t photosynthesise. They are where fertilisation takes place. Once a gametophyte has been fertilised, it develops into the above-ground ‘adult’ phase called a ‘sporophyte’. The sporophyte is where photosynthesis takes place. Gametophytes are only able to survive underground because they are supplied with carbon via mycorrhizal networks, shared with the adult sporophytes. So it's a kind of parental care where the previous generation is nourishing the next generation via the fungal networks.

This has also been shown in tree seedlings, where the seedlings are fed by the surrounding adult trees via fungal networks, right?

Yes. You can think of these examples as partial mycoheterotrophy.

This is really interesting. I always thought of mycoheterotrophic plants as achlorophyllous plants, but it's not true. There is a big range of mycoheterotrophism from partly photosynthetically active plants to the white, achlorophyllous ghost plants in the forest understory, which solely rely on carbon supplied by fungal networks.

Exactly, for example, all orchids are mycoheterotrophic at some point in their life. Some of them are mycoheterotrophic for their whole lives, and some just for the beginning.

I'm also interested in how mycoheterotrophic relationships are affecting the fungi involved. We think about mycoheterotrophs as not giving anything back to the fungus, but I wonder if there are other ways that the fungus is benefiting from this association, outside the formal exchange of nutrients. Might the fungus benefit from the shelter provided by roots, for example? This is very hard to know because you'd have to measure the effect of the mycoheterotroph on the fungus’s fitness, which is very hard to do in practice.

You mentioned that you used these mycoheterotrophic plants as indicators for the mycorrhizal symbiosis in a field experiment?

Yes, we found that in a long term fertilisation experiment where phosphorus, nitrogen and potassium were being added in a factorial combination, that wherever phosphorus was added, there were no mycoheterotrophs present. And in other plots where there was no phosphorus added, there were hundreds of mycoheterotrophic plants. It was a very strong effect –you could see it just walking around in the forest without doing any statistics.

So I sequenced the fungal communities in the soil, and found the fungi that the mycoheterotrophs partnered with were still present in the phosphorus plot. They were reduced in abundance somewhat, but they were definitely present. It seemed to me that the operation of the symbiosis was changing under the phosphorus regime.

This is surprising for me. I thought that you found a classical mycorrhizal response under the phosphorous regime where the trees started to reduce the amount of carbon provided to the fungus that then indirectly affected the mycoheterotrophic plant. But you said that the fungus was still there?

There was definitely a reduction in the abundance of the fungus, but the fungi was still present. If this reduced fungal abundance was responsible for the effect you'd expect to see a reduction in mycoheterotrophs rather than total absence. And so the complete absence suggested that the symbiosis starts to behave differently. But it struck me that this raised interesting possibilities, because if the big trees were reducing the carbon supply to the fungi and the fungi were then under more carbon limited conditions, but still persisting, then why would the mycoheterotrophic plants not be able to survive? Could the fungus make some kind of decision that would block the mycoheterotrophs from plugging in? And if it could make that kind of decision, why wouldn’t it do that all the time?

This finding I find very interesting because it may points to the exchange of luxury goods within the fungal networks. If you think of the natural condition in your experiment, there is this strong interaction of both partners, trees and mycorrhizal fungi. So there's a vital exchange of carbon versus nutrients such as phosphorus. In this case, where the symbiosis is important and very active, there is a constant carbon supply to the fungus and there isn't enough phosphorus supply to the trees – the ideal symbiotic situation. And whether the fungi are limited in nutrient access nor the trees in carbon, which are therefore luxury goods. So and then a tiny mycoheterotrophic plant can plug in and get some carbon out of the network because there is enough of everything, right? So the fungus would have to restrict the access to the network for the mycoheterotrophic plant, which would also be an extra effort. Then you can say, why should the fungus fight against the invader, because there is anyway enough carbon coming from the trees. Right? So then, there would be no disadvantage, whether for the fungi nor for the tree, to have a third partner who is kind of hitchhiking and get the carbon for free. In a way, this already makes sense. Still, then on top you mentioned the point of mycoheterotrophs may giving shelter to the fungus. I think there were even some studies showing that some vitamins are supplied by the mycoheterotrophic plants to the fungus, which are benefits that not have been accounted for in the carbon for nutrient calculation.

Yeah, I've heard this. I haven't seen any detailed work on it. And I know there are similar things that happen in other types of symbiosis. And it's definitely possible. I think the luxury goods perspective is really important, because we often think about these relationships as being very competitive and very strictly policed, as if everything was scarce. But there's actually quite a lot of carbon sloshing around in a lot of these systems, leaking out of roots. Maybe the members of these communities aren’t always so strict with each other.

But still, plants respond to changes in nutrient availability, for example when availability increases and the plants are no longer dependent on the fungal partner, as you just explained. Even the trees - which have almost free access to carbon through photosynthesis - reacted when you added phosphorus and your indicator for symbiosis, the mycoheterotrophs, disappeared. Do you think this reaction has something to do with resource exchange, or are there also other ways in which the treatments could affect symbiosis and the mycoheterotrophs in your experiment? Fertilisation can also be seen as an anthropogenic impact that could have imbalanced the natural system that evolved over millions of years under these nutrient conditions, causing this response. How do you see the symbiosis response in this experiment?

I think it has to do with resource exchange and how adding phosphorus changes the dynamics between photosynthetic plants and their fungal partners. And we know that if you do this in very controlled lab experiments, like the biological market research, exchange patterns can be very intricately managed. And flexible – if you do something, the balance might shift, and if you change something else, the balance might shift again. And so we know that these exchanges are dynamic, even if they don't always behave according to mycorrhizal markets.

Yes, I like all those experiments where they could show under laboratory conditions that the exchange of carbon for nutrients is fairly regulated. A fungus gets more carbon from the plant when the plant provides more nutrients, and vice versa. Such mechanisms also play an important role under natural conditions. But there must be other mechanisms or other rules. If we only had the market-like exchange of carbon for nutrients, then mycoheterotrophic plants would not have been allowed to develop. As you mentioned, there are even feedbacks across generations - that one generation feeds the next generation in mycorrhizal networks. This could be a market-relevant reward, but I just don't see how such exchange should be controlled instantly.

I’ve always wondered with biological markets, how exactly is a plant able to control how much carbon it provides to a given fungus? Suppose you have a plant root, and you have five different mycorrhizal fungi growing into the root. How is the plant able to regulate or to sanction one of those species and not the other three or other four species? It seems that arbuscule degradation and digestion is one way. Still, it does imply very fine sensing of who's where and who's doing what, and I'm interested in that. Have you heard anything new about how that might happen?

I think there is no proof so far, and it is not known how the exchange could be fine-tuned on a cell level. This would be needed to distinguish between different fungi colonising the same piece of roots. The plant would have to know which fungus provides how much of phosphorus or other resources, services.

And that's why I like mycoheterotrophic plants because they clearly show that other resource exchange mechanisms must play an important role in these large fungal networks. I like the analogy of the surplus or the luxury good as a counter concept. Particularly for trees as they assimilate enormous amounts of carbon. Up to 20% is exudated into the soil. I doubt that all of the carbon allocations to the soil are directed and controlled by market rules. We could show such patterns in a experiment we did with two plants under controlled greenhouse conditions. We used this very artificial system with just two plants to look at how plants exchange carbon for nutrients when sharing a fungal network with each other or hosting the fungus alone. We could see that one of the plants, sorghum, which is known to be very efficient in assimilating carbon by photosynthesis - it is probably under good light condition, seldom carbon limited - didn't respond if there was a fungal partner or not. So sorghum just grew very well under these conditions and assimilated a big share of carbon to the fungal partner. But what sorghum got back from the symbiosis was tremendously different depending on if another plant was interconnected or not. So, of course, when sorghum was hosting the fungal network alone, they got all the nutrients provided by the fungus. But when sorghum shared the network with the little neighboring plant, flax, sorghum got only 4% of the total nutrients provided by the network. Most surprising was that even sorghum did not get anything from the fungal network in terms of nutrients, it still allocated a lot of carbon. Sorghum grew very well anyhow, and we could not detect any disadvantage in their fitness. To me, this was pretty striking. Sorghum probably does not need the fungus for nutrient acquisition, and has enough carbon through efficient photosynthesis. Maybe they just don’t care if the fungus is colonising the roots and how much carbon is allocated to the fungus. With this, the neighbouring plant's growth can be facilitated tremendously by sharing the luxury good – carbon - across mycorrhizal networks. And this was also the main message I took out of this experiment, that there is no need that everything has to be done in one to one exchange, the “tit for tat” behavior – so you only get as much as you provide – and that in nature we find an another understanding of resources. It is more about availability of resources, not necessarily about having them and owning the resource. It is more about do you need a resource? Or you don't need it?

I think this is such an important question. Because when I first think of tit for tat exchange, I think of there being only two partners involved - one fungus, one root tip. But in reality, you have a fungus, which might be connected to several plants, and you have each plant connected to multiple different fungi. And so you have overlapping networks, and it's not one to one. How are all of these trading patterns integrated across larger networks and across larger areas? There has been some interesting work recently by Toby Kiers and her team about how fungi can move phosphorus around their networks from areas of plenty to areas of scarcity.

I personally never understood in the context of biological market theory, which advocates that “tit for tat” exchange, why other organism behaviour should have evolved with a concept is just 10,000 years old, right? I mean, the markets, they just exist since we have possession, settlements and trade. Of course, we live now in a world that is dominated by market situations and “tit for tat” rules, but why should be this also the dominating form of interaction in nature as well. I don't get it - but I'm not an evolutionary biologist.

Yes, it seems that even among human societies there are a variety of different types of economy, where value is attributed in different ways. My understanding of the biological market frameworks is that they can help build models which make predictions, which are important experimental tools. The models may turn out to be false, but they may turn out to be true. It just helps us to unpick the dynamics a bit more.

So if the mycorrhizal exchange cannot fully be explained by human market dynamics, could we learn something from the exchange of surplus, luxury goods?

I just read an article today talking about how much food is wasted, and it's a third of all food produced. It's astonishing how much this is - if food waste was a country, then its carbon emissions would place it in the top 10 countries in the world. So it's incredible that this kind of hoarding and possession mentality leads us into situations of great waste, which is not generally what you find in the living world. Waste seems to be a very human concept.

Another interesting point of fungi that you raised in your book is that the life of fungi is very entangled. One question in this respect, how difficult is it to define where a fungus, a fungal entity, begins and ends? Right. So ultimately, the definition of an individual in the fungal world is very different from our understanding. And this less clear definition of individuals probably also makes it hard to define whether fungi get a fair trade in resource exchange with a plant. So how do you see the definition of a fungal individual in general? You explored this in your book - can you define what an individual looks like for a fungi and these networks?

I think it's a really important question. The idea of individuals becomes very confused when we think about fungi and fungal networks. And this is one of the problems for biological market models. For those models, you have to identify individuals because you need to identify individual traders. But how do you decide what counts as a single trader? Is it one root tip, or one hyphal tip, or one clump of a network? Or a complete, intact network?

But what is your perception of a fungal individual then?

I don't really have a clear perception of a single individual. If you look at the level of the genome you can talk about about genetically identical individuals that form networks. Still, you can have nuclei moving around these networks in quite fluid ways. And it's not always easy to tell even genomically what an individual is. And so then you might think what about an individual as based on its coordinated behaviour, but different sides of the network might be behaving in quite different ways. One end of a network might be coupled with roots of one type of plant and the other side of the network with the roots of a different type of plant and say, a mycorrhizal fungus with birch fungus might be receiving from the fir and giving the birch and then later in the season, receiving from the birch and giving to the fir. This is a very different type of relationship going on simultaneously, one of giving or receiving. It’s not straightforward to talk about individuals based on their development either, because fungal networks are continually revising themselves and continually die and grow back – there's no consistent morphology like we have in our own bodies.

But if we now go back to the question, what is important for a fungus's fitness, and which boundaries are defining it? That's really hard to define. As you said, they probably associated to different plants, and the fungal network's connectedness is also modular, meaning that maybe there's some sort of perturbation, and this former shared mycorrhizal network is separated into two individual networks. And what does this mean for the fitness of the fungus?

I think this is one reason why fungi are so exciting for us to explore as humans because they confuse so many of our concepts. It's healthy for us to be puzzled by these organisms and to find them hard to understand. Ecology is about the relationships between organisms. And a lot of the time, you have organisms that relate in moments of contact, like a bee visiting a flower, for example. But bees and flowers don't form a physical connection between themselves. Fungi do. And so they seem to me to be poster organisms for ecological thinking. And they remind us that this is just how life works: you can't really understand any living organism as disconnected from its environment. And so I guess that fungi lead us into a much more fairly ecological worldview where the boundaries between all individuals start to blur.

But although it seems unclear what a fungal individual really is and how to define its boundaries, these fungal networks, the fungal hyphae growth, must obviously have some kind of perception of their extent. In your book you describe the development of a fungi around a wooden cube. Maybe you can explain that a bit more, because it's super fascinating. Even if it's not clear what the individual is, does the fungi have some kind of understanding of its distribution in space?

Yes, there's some kind of integration across the network. The experiment you mention was conducted by Lynne Boddy and her colleagues. They put a block of wood with a wood rotting fungus in it, and placed the wood block with the fungus growing inside on a petri dish. The fungus grew outward from the block of wood in a kind of exploratory pattern. But then when one part of that exploratory network, which looks like a fuzzy white circle, enountered another block of wood, then the fungus strengthened the connection with the new block of wood and withdrew from the other places it's been exploring. And so, just in a few weeks, the fungus completely remodels the network to form a strong connection between the two blocks of wood with the other fruitless avenues of exploration pruned back. And so you really see that even though it's hard to work out what's an individual, this network does behave like a coherent whole.

Is there anything clear about how the fungus is coordinating this behaviour?

Well, it's still not clear. There are several possibilities. There is an oscillatory flow through the network. The hydrodynamic process of flow could be a cue that keeps the fungus in touch with itself. It might also be due to chemicals flowing as part of that that hydrodynamic system. But then there can be phenomena that happen too fast for that. So one possibility is electrical signalling, which is a very underexplored possibility.

Which then makes these fungal networks very similar to brains, right? Because brains also rely on electric signals.

Precisely. Brains didn't evolve their tricks from scratch. And we now know that many organisms use electrical signals to coordinate their behaviour. Even bacterial colonies - a collection of single-celled organisms - can still conduct waves of electrical activity across the colony to allow certain types of signalling to take place. So our brains aren’t unique in their ability to transmit electrical signals, they’ve just made it really fast and complex. But these traits reflect very ancient, basic processes present in many living systems.

This makes me think that maybe the signalling could define a fungal individuum, even if it's dispersed and spread in complex networks. I mean, if the signal is transported from one end to the other, then it has to be the same individual, right? How do you see this?

Exactly. But you can also imagine a situation where you have a fungus connected to a plant connected to another fungus and signals moving along the fungal connections from plant to plant. And then, you can imagine a situation where rather than just a signal passing from plant A to B, that it might finds the path through another fungal network to plant C, or even plant D. If a signal could pass through several different fungal networks, which are not necessarily directly connected to each other it could, in principle, travel through an entire forest.

Terms:

Mycorrhiza is the term used to describe a form of symbiosis between fungi and plants in which a fungi forms a close association with the roots of a plant and forms specific organs. The mycorrhizal fungi mainly supply the plant with nutrients such as phosphate as well as water and in turn receive part of the energy-rich carbon compounds, such as sugars or lipids, produced by the photosynthesis of the (green) plants.

Mycoheterotrophy refers to the relationship between certain plant species and mycorrhizal fungi in which the plant obtains all or part of its nutrition through parasitism on fungi rather than photosynthesis.

Within biological market frameworks, the exchange of resources and services between organisms is analysed from a market perspective, with individuals making strategic trade investments to maximise market gains. In this way, organisms should be able to reduce the supply of resources to a partner with an inferior offer and instead allocate supply to a better partner - in the sense of “tit for tat”.

This interview was conducted for the publication of the "Body Extravagant" exhibition at Pilz Welle Lust 2020 in Basel.