Unravelling nature's complex tapestry: plant community stability and soil microbial networks

Plants associate with complex interactive networks of soil microbial communities. We show that plant community stability is associated with a decoupling of prokaryote and fungal soil networks. Prokaryote-fungal decoupling occurred in soil abandoned from agriculture 60 years prior to our study.
Unravelling nature's complex tapestry: plant community stability and soil microbial networks
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The world around us is teeming with plant life. Plant life forms the foundation of all terrestrial ecosystems, from towering forests to vibrant meadows. The beauty and complexity of plant life has been celebrated for millennia. Dating back more than 3000 years, reverence of plant life is evident: in a remarkably preserved mural in a home on the Greek island Santorini from c. 1500 BC one of the oldest recognisable botanical paintings likely marks the very beginning of the celebration of plant life in art (Fig 1a). Now, the natural world is at a critical tipping point, threatened by the combined and interconnected threats of climate change, biodiversity loss and land-use change (Fig 1b). In the face of these pressing challenges, understanding and safeguarding the stability of plant communities has become paramount to mitigate the impacts of global change.

Figure 1 (a) a reverence of plant life dating back to approximately 1500 BC, found on a mural in a house on the Greek island Santorini (Photograph: akg-images/De Agostini Picture/Phaidon), (b) Mountains of Sea by Hanneke van Ryswyk depicting the power of global change driven extreme flooding events (https://www.hannekevanryswyk.com/).

Figure 1 (a) A reverence of plant life dating back to approximately 1500 BC, found on a mural in a house on the Greek island Santorini (Photograph: akg-images/De Agostini Picture/Phaidon), (b) Mountains of Sea by Hanneke van Ryswyk depicting the power of global change driven extreme flooding events (https://www.hannekevanryswyk.com/).

Much of the beauty and wonder we attribute to the natural world lies in what is visible above ground, but beneath our feet lies a world teeming with a diversity of hidden life (Fig 2a). A teaspoon of soil contains more living organisms than humans on earth, including a billion bacterial cells and two hundred meters of fungal hyphae (Fig 2b). Soil bacteria and fungi are the engines of soil resource cycling, forming a critical cog in the wheel of the turnover of dead plant material into plant-available nutrients; ultimately shaping the vibrant plant life that unfolds above ground. Connecting the role of soil microbiota to above ground processes is inherently challenging, owing to the sheer diversity and complexity of soil microbial life. However, it is this diversity and complexity that are predicted to play a critical role in how the soil microbial community governs ecosystem stability. To specifically capture this diversity and complexity of the soil microbial community, we used a network science approach and addressed the challenge of connecting belowground microbial network topology to plant community stability in a 13-year mesocosm experiment.

Figure 2 (a) The diversity of soil life depicted by María Fernández-Bravo (Instagram: @mariafernandez_watercolors, Twitter: @MariaFndzBravo), and (b) the intricate networks of plants and fungi in soil depicted by Dina in ‘t Zandt (Twitter: @Dina_intZandt).

Truth be told, the mesocosm experiment was never supposed to happen and was an unlikely candidate to continue for 13 years. During her postdoctoral research, my supervisor Zuzana Münzbergová set up this experiment to study grassland establishment dynamics, a topic close to her heart, but an endeavour that was nevertheless faced with resistance and scepticism. Zuzana did it anyways, establishing 60 plant species-rich, dry grassland communities on two distinct soils: soil from a natural grassland site, and soil from a site that had been abandoned from agricultural practises six decades prior to the start of the experiment (Fig 3a, b). After 3 years, she decided to continue monitoring the mesocosms for ‘a few more years’. After 9 years, it was decided the mesocosms were not going to yield any more interesting results and were occupying too much space. A request was made to the gardening team to dispose of the mesocosms. However, the gardening team decided they liked the diversity of flowering plants and preserved the mesocosms as an ornamental piece in the experimental garden. The following year, above ground measurements were resumed. Finally, after 13 years and driven by the wish to develop a microbial research line within the Population Ecology department, soil microbial samples were taken from the mesocosms. Perhaps the shifts in above ground plant biomass over the 13 years could be linked with belowground microbial communities?

Figure 3 (a) A mesocosm plant community in the first year of the experiment (Photograph: Zuzana Münzbergová), (b) the mesocosm communities after 13 growing seasons (Photograph: Tomáš Dostálek).

Soil microbial networks showed strikingly different topologies between the natural grassland and abandoned arable soil communities. In natural grassland soil, prokaryote and fungal networks were decoupled, showing independent responses of prokaryote and fungal communities (Fig 4a). Conversely, in abandoned arable soil, prokaryote and fungal networks were coupled, showing interconnected dynamics (Fig 4b). This is remarkable given that the abandoned arable soil had not experienced agricultural practices for 60 years prior to collection, was thoroughly homogenised to break up any below ground networks prior to the experiment, and was sown with the identical plant community. Thus, this long-term legacy of past agricultural practices emphasizes the enduring impact of human activities on below ground dynamics. Additionally, it serves as a stark reminder of the irreversible consequences that can arise from disturbing below ground soil systems. Our findings therefore highlight, echoing previous studies, the urgency of conservation and sustainable practices as human activities have pervasive effects on belowground ecosystems.

Figure 4 (a) In stable settings, prokaryotes (circles, black border) and fungi (pentagons, white border) occurred in separately responding clusters of the networks. In such decoupled networks, the spread of local disturbance effects are likely buffered as effects on a subset of taxa are not likely to spread to unconnected taxa (red arrows showing the spread among connected taxa). (b) In unstable settings, prokaryotes and fungi respond in tandem and create three dominant clusters. The resulting microbial networks are likely to spread disturbance effects throughout large parts of the network given the high connectiveness of dominant groups (red arrows).

Strikingly, high temporal stability above ground was linked to a decoupling of prokaryote and fungal networks below ground. This means that plant communities with a low fluctuation in above ground productivity over time were associated with soil prokaryote and fungal communities showing independent responses (Fig 4a). Conversely, plant communities with a high fluctuation in above ground productivity over time were associated with soil prokaryote and fungal communities with interconnected dynamics (Fig 4b). To understand this correlation, we had to understand what drives robustness of complex systems; a system is robust when it sustains its basic function despite change or failures occurring in part of its components. For example, many ecosystems do not immediately collapse when one or multiple species are lost, they remain functional despite the loss of part of their components. Robustness of complex systems is related to the connectivity of the components. A high connectivity of components can be positive, think about the efficient travel of information among a large network such as computers connected via the world wide web. However, being part of such a connected network has its catch: connectivity creates vulnerability. While information may travel efficiently, computer viruses do so too, easily infecting many computers connected to the world wide web (Barabási and Pósfai, 2016, Network Science, Cambridge University Press). Translated to our coupled prokaryote and fungal networks, this means that a local perturbation affecting a few microbiota can easily spread, cascading to other areas of the below ground network (Fig 4b). However, when prokaryote and fungal networks are decoupled, locally unconnected subgroups of prokaryotes and fungi occur. These subgroups buffer against the propagation of changes in the network, creating stability in the natural grassland soil communities (Fig 4a). Imagine a group of islands with inhabitants where changes in the number of inhabitants on one island does not affect the number of inhabitants of another islands as bridges or other connections are missing.

 Our findings uncover exciting new avenues to understand and protect the mechanisms safeguarding community stability as well as promising aspects to consider in conservation and restoration of natural communities. From ancient celebrations of the plant world to modern-day scientific discoveries, the diverse and complex nature of the natural world is captivating and there is astonishing order to a seemingly chaotic system.

 Though this be madness, yet there is method in t - William Shakespeare, Hamlet

 Let us hope that through responsible land management, conservation efforts, and a collective commitment to reducing disturbances, the wonders of nature will continue to inspire the generations to come.

Acknowledgements

I am grateful to Natalie J. Oram, Zuzana Münzbergová and Zuzana Kolaříková for their valuable suggestions to this blog. All displayed artwork is used with the artists’ kind permission and is a selection of work from the art-science exhibition ‘Below Ground: Soil life in a changing climate’ at the Irish Agricultural Museum, curated by Natalie J. Oram in collaboration with Dina in ‘t Zandt and John Finn (https://nataliejoram.wordpress.com/below-ground-soil-life-in-a-changing-climate/). This is with exception of Fig 1a.

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