Biology subjects

Kiers, E. T.

Publications and source records attributed to Kiers, E. T..

5 recordsLinked to original sources

bioRxiv2025

Carbon-phosphorous exchange rate constrains growth of arbuscular mycorrhizal fungal networks

Symbiotic nutrient exchange between arbuscular mycorrhizal (AM) fungi and their host plants varies widely depending on their physical, chemical, and biological environment. Yet dissecting this context dependency remains challenging because we lack methods for tracking nutrients such as carbon (C) and phosphorus (P). Here, we developed a new approach to quantitatively estimate C and P fluxes in the AM symbiosis from comprehensive network morphology quantification, achieved by robotic imaging and machine learning based on roughly 100 million hyphal shape measurements. We found that rates of C transfer from the plant and P transfer from the fungus were, on average, related proportionally to one another. This ratio was nearly invariant across AM fungal strains despite contrasting growth phenotypes, but was strongly affected by plant host genotype. Fungal phenotype distributions were bounded by a Pareto front with a shape favoring specialization in an exploration-exploitation trade-off. This means AM fungi can be fast range expanders or fast resource extractors, but not both. Manipulating the C/P exchange rate by swapping the plant host genotype shifted this Pareto front, indicating that the exchange rate constrains possible AM fungal growth strategies. We show by mathematical modeling how AM fungal growth at fixed exchange rate leads to qualitatively different symbiotic outcomes depending on fungal traits and nutrient availability.

biophysics↗

bioRxiv2024

The evolution of signalling and eavesdropping in plant-fungal networks

Experiments have shown that when one plant is attacked by a pathogen or herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We examined the evolutionary plausibility of this and other hypotheses theoretically. We found that the evolution of plant signalling about an attack requires restrictive conditions, and so will rarely be evolutionarily stable. The problem is that signalling about an attack provides a benefit to competing neighbours, even if they are kin, and so reduces the relative fitness of signalling plants. Indeed, selection is often more likely to push plant behaviour in the opposite direction - with plants signalling dishonestly about an attack that has not occurred, or by suppressing a cue that they have been attacked. Instead, we show that there are two viable alternatives that could explain the empirical data: (1) the process of being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to fully suppress; (2) mycorrhizal fungi monitor their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network. Our results suggest the empirical work that would be required to distinguish between these possibilities. Significance statementExperiments have shown that when one plant is attacked by a herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We found theoretically that plant warning signals are rarely evolutionarily stable. Instead, we identify two viable alternatives that could explain the empirical data: (1) being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to suppress; (2) mycorrhizal fungi monitor their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network.

evolutionary biology↗

bioRxiv2023

Hyphal exploration strategies and habitat modification of an arbuscular mycorrhizal fungus in microengineered soil chips

Arbuscular mycorrhizal fungi (AMF) are considered ecosystem engineers, however, the exact mechanisms by which they modify and influence their immediate surroundings are largely unknown and difficult to study in soil. In this study, we used microfluidic chips, simulating artificial soil structures, to study foraging strategies and habitat modification of Rhizophagus irregularis in symbiotic state associated to carrot roots. Our results suggest that AMF hyphae forage over long distances in void spaces, prefer straight over tortuous passages, anastomose and show strong inducement of branching when encountering obstacles. We observed bi-directional vesicle transport inside active hyphae and documented strategic allocation of biomass within the mycelium e.g., truncated hyphal growth and cytoplasm retraction from inefficient paths. We found R. irregularis able to modify pore-spaces in the chips by producing irregularly shaped spores that filled up pores. We suggest that studying AMF hyphal behaviour in spatial settings can explain phenomena reported at bulk scale such as AMF modification of water retention in soils. The use of microfluidic soil chips in AMF research opens up novel opportunities to under very controlled conditions study ecophysiology and interactions of the mycelium with both biotic and abiotic factors.

microbiology↗

bioRxiv2020

Parallel evolution in the integration of a co-obligate aphid symbiosis

Insects evolve dependencies - often extreme - on microbes for nutrition. These include cases where insects harbour multiple endosymbionts that function collectively as a metabolic unit. How do these metabolic co-dependencies originate, and is there a predictable sequence of events leading to the integration of new symbionts? While dependency on multiple nutrient-provisioning symbionts has evolved numerous times across sap-feeding insects, there is only one known case of metabolic co-dependency in aphids, between Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily. Here we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. A comparison of recent and ancient associations allows us to investigate intermediate stages of metabolic and physical integration between the typically facultative symbiont, Serratia, and the ancient obligate symbiont Buchnera. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner, through parallel evolutionary processes. Specifically, we show (i) how the repeated losses of the riboflavin pathway in Buchnera leads to dependency on Serratia, (ii) evidence of a stepwise process of symbiont integration, whereby dependency evolves first, then essential amino acid pathways are lost (at ~30-60MYA), which coincides with increased physical integration of the companion symbiont; and (iii) dependency can evolve prior to specialised structures (e.g. bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesising nutrients may provide a unified explanation for the sequence of gene loses that occur during the evolution of co-obligate symbiosis.

evolutionary biology↗

bioRxiv2018

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases where two species cease to cooperate, and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways towards breakdowns of the mutualism between plants and arbuscular mycorrhizal (AM) fungi. Using a comparative approach, we identify ~25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants either: (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.\n\nSignificance StatementCooperative interactions among species - mutualisms - are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms breakdown? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyse two potential trajectories towards evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost - but only if successful alternatives evolve.

evolutionary biology↗