Noncircadian oscillations in amino acid transport have complementary profiles in assimilatory and foraging hyphae of Phanerochaete velutina

Abstract

Summary• Cord-forming woodland basidiomycete fungi form extensive, interconnected mycelial networks that scavenge nitrogen (N) efficiently. We have developed techniques to study N dynamics in such complex mycelial systems in vivo .• Uptake and distribution of the nonmetabolised, 14 C-labelled amino-acid analogue, α -aminoisobutyrate ( 14 C-AIB) was continuously imaged in Phanerochaete velutina growing across scintillation screens using an enhanced photon-counting camera.• Oscillations in the 14 C-AIB signal were observed for both the assimilatory hyphae in the inoculum and the foraging hyphae, but with complementary profiles. Pulses were asymmetric, with an abrupt switch between each exponential decay phase and the next rising phase. The period of the oscillations was 16 h at 21 ° C, but showed a strong temperature dependence with a temperature coefficient of 2.1. Oscillations occurred in the absence of obvious pulses in growth.• Some, but not all, of the features of the oscillations were simulated using a model of amino acid accumulation and transport that included both vacuolar uptake, and release once an intravacuolar concentration threshold was exceeded. The combination of imaging and modelling provides a useful framework to understand N fluxes in vivo .

New approaches to investigating the function of mycelial networks

“…Once these have reached a threshold level, a proportion of the amino acid would be released into a pathway for mass flow to the growing hyphae at the colony margin. A computer simulation model was constructed incorporating partial differential equations describing the concentration dependence of these processes, which generated a comparable pulse pattern to that observed when values based on physiological data were used for amino acid transport rates across plasmalemma and tonoplast (Tlalka et al, 2003). Whether such a model is sufficient to explain all the experimental data remains to be established, however, at this stage it is consistent with the vacuole as a key compartment in amino-acid dynamics in mycelial fungi.…”

“…On more detailed examination, the shape of the pulses was highly asymmetric, with an apparent switch between a gradual rise and a sudden drop in the intensity of the amino acid signal during each cycle. Furthermore, exactly the opposite profile was observed from the assimilatory hyphae growing on the inoculum compared to those that were foraging (Tlalka et al, 2003;Fig 6). This suggested one plausible sequence of events to explain these data that is consistent with evidence for amino acid transport systems in the literature.…”

Network Automata: Coupling Structure and Function in Dynamic Networks

“…We have demonstrated the practicability of the framework by applying it to a class of biologically inspired models, which produce qualitatively similar canalised flow patterns to those observed in real woodland fungi [15,16,17,19]. This suggests that for organisms that have to adapt their morphology to a variable environment, function may play a crucial role in determining structure.…”

“…This is depicted explicitly in Table I. The result of such a delay is the build up of resource towards the periphery of the object as one might expect [15]. This is illustrated in Fig.…”

“…5 and emergent canalized flux channels are clear. Such channels have been observed experimentally in a wide class of real biological fungi [15]. In Rulesets a and b, the physical transport of nutrient is of comparable speed to that of the growth, which is clearly not reasonable for most biological systems.…”