Bidirectional Propagation of Signals and Nutrients in Fungal Networks via Specialized Hyphae

Schmieder, Stefanie S.; Stanley, Claire E.; Rzepiela, Andrzej J.; Swaay, Dirk van; Sabotič, Jerica; Nørrelykke, Simon F.; deMello, Andrew J.; Aebi, Markus; Künzler, Markus

doi:10.1016/j.cub.2018.11.058

Cited by 83 publications

(52 citation statements)

References 55 publications

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“…Evolutionarily speaking, this proposed mechanism is intermediate between the cytoskeleton-mediated mechanosensing of mammalian cells and cell wall-reliant mechanosensing of bacteria and plants, particularly related to osmolarity stress and loss of turgor pressure. In fact, fungal hyphae have been observed to grow in an oscillatory manner and bidirectionally transmit signals tied to pathogen attack and nutrient sources (Schmieder et al, 2019). Physarum may have optimized this inherent ability to execute information processing more rapidly.…”

Section: Computational Modeling Of Mass Sensingmentioning

confidence: 99%

Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism

Murugan

Kaltman

Jin

et al. 2020

Preprint

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Running title:Mechanical force sensing underlies Physarum aneural cognition AbstractThe unicellular protist Physarum polycephalum is an important emerging model for understanding how aneural organisms process information toward adaptive behavior. Here, we reveal that Physarum can use mechanosensation to reliably make decisions about distant objects its environment, preferentially growing in the direction of heavier, substrate-deforming but chemically-inert masses. This long-range mass-sensing is abolished by gentle rhythmic mechanical disruption, changing substrate stiffness, or addition of a mechanosensitive transient receptor potential channel inhibitor. Computational modeling revealed that Physarum may perform this calculation by sensing the fraction of its growth perimeter that is distorted above a threshold straina fundamentally novel method of mechanosensation. Together, these data identify a surprising behavioral preference relying on biomechanical features and not nutritional content, and characterize a new example of an aneural organism that exploits physics to make decisions about growth and form. Highlights The aneural Physarum makes behavioral decisions by control of its morphology  It has a preference for larger masses, which it can detect at long range  This effect is mediated by mechanosensing, not requiring chemical attractants  Machine learning reveals that it surveys environment and makes decision in < 4 hours  A biophysical model reveals how its pulsations enable long-distance mapping of environmental features A defining feature of any living organism is its ability to select actions that maximize utility in diverse environments (Barandiaran and Moreno, 2006). Decision-making is a process that is well-characterized in behavioral studies of human and other vertebrate species possessing nervous systems. Increasingly, it is also recognized as a fundamental capability whose evolutionary roots extend to the most basal forms on the tree of life (Baluška and Levin, 2016;Lyon, 2006Lyon, , 2015. Even unicellular organisms, including bacteria, have been studied as computational systems that collect information from their environment and use it to guide subsequent behaviors (Balazsi et al.

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Section: Computational Modeling Of Mass Sensingmentioning

confidence: 99%

Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism

Murugan

Kaltman

Jin

et al. 2020

Preprint

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“…Perhaps, filamentous fungi can perceive the sound of hyphal grazers. There would be advantages of vibration detection as a warning signal: the fungal mycelium could avoid advancing into areas of intense animal activity, for example of collembola or earthworms (the distribution of animals in soil tends to be quite clustered), or the fungus could mount defense-related actions (induced defense) when it encounters an impending attack by microarthropods or nematodes [10]. Beyond avoidance in space and upregulation of defense, a third possible fungal response to sound could be increased sporulation.…”

Section: How Sound Might Carry Useful Information For Soil Biotamentioning

confidence: 99%

Sounds of Soil: A New World of Interactions under Our Feet?

Rillig

Bonneval²,

Lehmann

2019

Soil Systems

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Soils are biodiversity-dense and constantly carry chemical flows of information, with our mental image of soil being dark and quiet. But what if soil biota tap sound, or more generally, vibrations as a source of information? Vibrations are produced by soil biota, and there is accumulating evidence that such vibrations, including sound, may also be perceived. We here argue for potential advantages of sound/vibration detection, which likely revolve around detection of potential danger, e.g., predators. Substantial methodological retooling will be necessary to capture this form of information, since sound-related equipment is not standard in soils labs, and in fact this topic is very much at the fringes of the classical soil research at present. Sound, if firmly established as a mode of information exchange in soil, could be useful in an 'acoustics-based' precision agriculture as a means of assessing aspects of soil biodiversity, and the topic of sound pollution could move into focus for soil biota and processes.

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“…However, the response rapidly spread from those chambers, recruiting the whole fungus into a network-wide response. This response didn't travel along every hypha, however, but was confined to a few hyphae (which Schmieder et al [7] identified as a special class of propagating hyphae), on which the signal traveled at a speed of about 5 mm/s. Even more remarkably, signals did not simply travel toward the edge of the network, but also traveled (at similar speeds!)…”

mentioning

confidence: 99%

“…Previous work from Markus Kü nzler's group showed that, when nematodes graze upon C. cinerea, the fungus responds by releasing a host of chemical weapons [6]. Now, in a new study published recently in Current Biology, this group has shown how the whole fungal network is mobilized to produce these chemical defenses [7].…”

mentioning

confidence: 99%

“…Understanding how fungal networks can transmit signals has been difficult because the cellular highways of fungi (the hyphae) are densely interconnected, making it very hard to confine any stimulus to a single part of the network. In the new work, Schmieder et al [7] used a passive microfluidic device -a set of transparent rubber chambers linked by narrow channels -to constrain the growth of the fungus. The fungus expands into a dense tangle of cells within the chambers, but, within the narrow channels between the chambers, the individual cellular strands are combed out, allowing individual lines of communication to be seen.…”

mentioning

confidence: 99%

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Fungal Biology: Bidirectional Communication across Fungal Networks

Roper

Dressaire

2019

Current Biology

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Bidirectional Propagation of Signals and Nutrients in Fungal Networks via Specialized Hyphae

Abstract: Graphical AbstractHighlights d Transport of signals and nutrients in fungal mycelia occurs via specialized hyphae d Transport in these hyphae is bidirectional d Direction of transport in these hyphae oscillates between acropetal and basipetal

Cited by 83 publications

References 55 publications

Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism

Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism

Sounds of Soil: A New World of Interactions under Our Feet?

Fungal Biology: Bidirectional Communication across Fungal Networks

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