Fungal sensing skin
FFungal sensing skin
Andrew Adamatzky a , Antoni Gandia b , Alessandro Chiolerio c,a a Unconventional Computing Laboratory, UWE, Bristol, UK b Mogu S.r.l., Inarzo, Italy c Center for Sustainable Future Technologies, Istituto Italiano di Tecnologia, Torino, Italy
Abstract
A fungal skin is a thin flexible sheet of a living homogeneous mycelium madeby a filamentous fungus. The skin could be used in future living architecturesof adaptive buildings and as a sensing living skin for soft self-growing/adaptiverobots. In experimental laboratory studies we demonstrate that the fungalskin is capable for recognising mechanical and optical stimulation. The skinreacts differently to loading of a weight, removal of the weight, and switchingillumination on and off. These are the first experimental evidences that fungalmaterials can be used not only as mechanical ‘skeletons’ in architecture androbotics but also as intelligent skins capable for recognition of external stimuliand sensorial fusion.
Keywords: fungi, biomaterials, sensing, sensorial fusion, soft robotics
1. Introduction
Flexible electronics, especially electronic skins [1, 2, 3] is amongst the mostrapidly growing and promising fields of novel and emergent hardware. The elec-tronic skins are made of flexible materials where electronics capable of tactilesensing [4, 5, 6, 7] are embedded. The electronic skins are capable of low levelperception [8, 9] and could be developed as autonomous adaptive devices [10].Typical designs of electronic skins include thin-film transistor and pressure sen-sors integrated in a plastic substrate [11], micro-patterned polydimethylsiloxanewith carbon nanotube ultra-thin films [12, 13], a large-area film synthesised bysulfurisation of a tungsten film [14], multilayered graphene [15], platinum rib-bons [3], Polyethylene terephthalate (PET) based silver electrodes [16], digitallyprinted hybrid electrodes for electromyographic recording [17] or for piezoresis-tive pressure sensing [18], or channels filled with conductive polymer [19].Whilst the existing designs and implementations are highly impactful, theprototypes of electronic skins lack a capacity to self-repair and grow. Such prop-erties are useful, and could be necessary, when an electronic skin is used in e.g.unconventional living architecture [20], soft and self-growing robots [21, 22, 23,24] and development of intelligent materials from fungi [25, 26, 27, 28]. Basedon our previous experience with designing tactile, colour sensors from slimemould
Physarum polycephalum [29, 30, 31] and our recent results on fungal
Preprint submitted to Journal Name August 25, 2020 a r X i v : . [ c s . ET ] A ug lectrical activity [32, 33, 34] we decided to propose a thin layer of homoge-neous mycelium of the trimitic polypore species Ganoderma resinaceum as alive electronic skin and thus investigate its potential to sense and respond totactile and optical stimuli. We call the fungal substrate, used in present paper,‘fungal skin’ due to its overall appearance and physical feeling. In fact, sev-eral species of fungi have been proposed as literal skin substitutes and tested inwound healing [35, 36, 37, 38, 39, 40].The paper is structured as follows. We introduce the protocol for growing thefungal skin and the methods of electrical activity recording in Sect. 2. Patternsof electrical activity of the fungal skin are analysed in Sect. 3. Results areconsidered in a wider context and directions of future studies are outlined inSect. 4.
2. Methods
Potato dextrose agar (PDA), malt extract agar (MEA) and malt extract(ME) were purchased from Sigma-Aldrich (USA). The
Ganoderma resinaceum culture used in this experiment was obtained from a wild basidiocarp foundat the shores of
Lago di Varese , Lombardy (Italy) in 2018 and maintained inalternate PDA and MEA slants at MOGU S.r.l. for the last 3 years at 4 º Cunder the collection code 019-18.The fungal skin was prepared as follows.
G. resinaceum was grown on MEAplates and a healthy mycelium plug was inoculated into an Erlenmeyer flaskcontaining 200 ml of 2% ME broth (MEB) that was then incubated undercontinuous shaking at 200 rpm and 28 o C for 5 days. Subsequently, this liquidculture was homogenised for 1 minute at max. speed in a sterile 1L Waringlaboratory blender (USA) containing 400 mL of fresh MEB, the resulting 600 mLof living slurry were then poured into a 35 by 35 cm static fermentation tray. Theslurry was let to incubate undisturbed for 15 days to allow the fungal hyphae tointer-mesh and form a floating mat or skin of fungal mycelium. Finally, a livingfungal skin c. 1.5 mm thick was harvested (see texture of the skin in Fig. 1a),washed in sterile demineralised water, cut to the size 23 cm by 11 cm andplaced onto a polyurethane base to keep electrodes stable during the electricalcharacterisation steps (Fig. 1b).The electrical activity of the skin was measured as follows. We used iridium-coated stainless steel sub-dermal needle electrodes (Spes Medica S.r.l., Italy),with twisted cables. The pairs of electrode were inserted in fungal skin (Fig. 1b).In each pair we recorded a difference in electrical potential between the elec-trodes. We used ADC-24 (Pico Technology, UK) high-resolution data log-ger with a 24-bit Analog to Digital converter, galvanic isolation and software-selectable sample rates. We recorded electrical activity with a frequency of onesample per second. We set the acquisition voltage range to 156 mV with anoffset accuracy of 9 µ V to maintain a gain error of 0.1%. For mechanical stimu-lation with 30 g nylon cylinder, contact area with the fungal skin was c. 35 mmdisc. For optical stimulation we used an aquarium light, array of LEDs, 36 whiteLEDs and 12 blue LEDs, 18 W, illumination on the fungal skin was 0.3 LUX.2 a) (b) P o t e n ti a l , m V (c) ca b d e f g h i j k l P o t e n ti a l , m V − − − − − −
20 Time, sec1.2 × × × (d)Figure 1: Recording of electrical activity of fungal skin. (a) Close-up texture detail ofa fungal skin. (b) A photograph of electrodes inserted into the fungal skin. (c) Trainof three low-frequency spikes, average spike’s width there is 1500 sec, a distance betweenspike peaks is 3000 sec and average amplitude is 0.2 mV. (d) Example of several train ofhigh-frequency spikes. Each train T xy = ( A xy , W xy , P xy ) is characterised by average ampli-tude of spikes A xy mV, width of spikes W xy sec and average distance between neighbouringspikes’ peaks P xy sec: T ab = (2 . , , T cd = (1 . , , T ef = (1 . , , T gh = (2 . , , T ij = (2 . , , T kl = (2 . , , . Results Endogenous electrical activity of the fungal material is polymorphic. Lowand high frequency oscillations patterns can emerge intermittently. A train offour spikes in Fig. 1c is an example of low frequency oscillations. Trains ofhigh-frequency spikes are exemplified in Fig. 1d.Electrical responses to tactile loading and illumination are distinctive. Anexample of several rounds of stimulation is shown in Fig. 2a. The fungal skinresponds to loading of a weight with a high-amplitude wide spike of electricalpotential sometimes followed by a train of high-frequency spikes. The skinalso responds to removal of the weight by a high-amplitude spike of electricalpotential.An exemplar response to loading and removal of weight is shown in Fig. 2b.The parameters of the fungal skin responses to the weight being placed on theskin are the following. An average delay of the response (the time from weightapplication to a peak of the high-amplitude spike) is 911.4 sec ( σ =1280.1, min-imum 25 sec and maximum 3200 sec). An average amplitude of the responsespike (marked ‘s’ in the example Fig. 2b) is 0.4 mV ( σ =0.2, minimum 0.1 mVand maximum 0.8 mV). An average width of the response spike is 1261.8 sec( σ =1420.3, minimum 199 sec and maximum 4080 sec), meaning that the averageenergy consumed per current unit, associated to the response, is approximately0.5 J/A. A train of spikes (marked ‘r’ in the example Fig. 2b), if any, followingthe response spike usually has 4 or 5 spikes. The fungal skin responds to removalof the weight (the response is marked ‘p’ in the example Fig. 2b) with a spikewhich average amplitude is 0.4 mV ( σ =0.2, minimum 0.2 mV and maximum0.85 mV). Amplitudes are less indicative than frequencies because an amplitudedepends on the position of electrodes with regards to propagating wave of ex-citation. An average width of the spike is 774 sec ( σ =733.1, minimum 100 secand maximum 2000 sec. A response of the fungal skin to removal of the weightwas not observed in c. 20% of differential electrode pairs. The average responsetime is 385.5 sec ( σ =693.3 sec, minimum 77 sec and maximum 1800 sec).Fungal skin’s response to illumination is manifested in the raising of the base-line potential, as illustrated in the exemplar recordings in Fig. 2c. In contrastto mechanical stimulation response the response-to-illumination spike does notsubside but the electrical potential stays raised till illumination is switched off.An average amplitude of the response is 0.61 mV ( σ =0.27, minimum 0.2 mV andmaximum 1 mV). The raise of the potential starts immediately after the illumi-nation is switched on. The potential reaches its maximum and goes onto plateauin 2960 sec in average ( σ =2201, minimum 879 sec and maximum 9530 sec).Typically, we did not observe any spike trains after the illumination switchedoff however in a couple of trials we witnessed spike trains on top of the raisedpotential, as shown in Fig. 2d. 4 oL*WoW*LoL*LoL*W* Wo W*W* L*LoWoWo P o t e n ti a l , m V − − × × × × (a) W* Wosr p P o t e n ti a l , m V × × × (b) L* Lo P o t e n ti a l , m V − (c) L* Lo P o t e n ti a l , m V (d)Figure 2: Fungal skin response to mechanical and optical stimulation. (a) Exemplar recordingof fungal skin electrical activity under tactile and optical stimulation. Moments of applyingand removing a weight are shown as ‘W*’ and ‘Wo’ and switching light ON and OFF as‘L*’ and ‘Lo’. (b) Exemplar response to mechanical stimulation. Moments of applying andremoving a weight are shown as ‘W*’ and ‘Wo’. High-amplitude response is labelled ‘s’. Thisresponse is following by a train of spikes ‘r’. A response to the removal of the weight is labelled‘p’. (c) Exemplar response of fungal skin to illumination, recorded on three pairs of differentialelectrodes. ‘L*’ indicates illumination is applied, ‘Lo’ illumination is switched off. (d) A trainof spikes on the raised potential as a response to illumination. timulus is applied Stimulus is removed ttVV Response to pressure/load Response to illumination (a) (b)Figure 3: (a) A scheme of the fungal skin responses to mechanical load and optical stimula-tions. (b) Slime mould
P. polycephalum response to application of 0.01 g glass capillary tube.Redrawn from [30].
4. Discussion
We demonstrated that a thin sheet of homogeneous living mycelium of
Gan-oderma resinaceum , which we named ‘fungal skin’, shows pronounced electricalresponses to mechanical and optical stimulation. Can we differentiate betweenthe fungal skin’s response to mechanical and optical stimulation? Definitely,see Fig. 3a. The fungal skin responds to mechanical stimulation with a 15 minspike of electrical potential, which diminishes even if the applied pressure on theskin remains. The skin responds to optical stimulation by raising its electricalpotential and keeping it raised till the light is switched off.Can we differentiate the responses to loading and removal of the weight?Yes. Whilst amplitudes of ‘loading’ and ‘removal’ spikes are the same (0.4 mVin average) the fungal skin average reaction time to removal of the weight is 2.4times shorter than the reaction to loading of the weight (385 sec versus 911 sec).Also ‘loading’ spikes are 1.6 times wider than ‘removal’ spikes (1261 sec versus774 sec).Fungal skin response to weight application is, in some cases, esp. Fig. 2y,similar to response of slime mould to application of the light weight [30]. Thefollowing events are observed (Fig. 3)b: oscillatory activity before stimulation,immediate response to stimulation, prolonged response to stimulation as a trainof high-amplitude spikes, return to normal oscillatory activity. This might in-dicate some universal principles of sensing and information processing in fungiand slime moulds.The sensing fungal skin proposed has a range of advantages comparing toother living sensing materials, e.g. slime mould sensors [29, 30, 31] electronicsensors with living cell components [41], chemical sensors using living taste,olfactory, and neural cells and tissues [42] and tactile sensor from living cellculture [43]. The advantages are low production costs, simple maintenance,durability. The last but not least advantage is scalability: a fungal skin patchcan be few microns and it can be grown to several metres in size.6n future studies we will aim to answer the following questions. Would it bepossible to infer a weight of the load applied to the fungal skin from patterns ofits electrical activity? Would the fungal skin indicate directionality of the loadmovement by its spiking activity? Would it be possible to locate the position ofthe weight within the fungal network? Would it be possible to map a spectrumof the light applied to the skin onto patterns of the skin’s electrical activity?
Acknowledgement
This project has received funding from the European Union’s Horizon 2020research and innovation programme FET OPEN “Challenging current thinking”under grant agreement No 858132.
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