Synchronization of oscillatory growth prepares fungal hyphae for fusion

Abstract
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Abstract

Communication is crucial for organismic interactions, from bacteria, to fungi, to humans. Humans may use the visual sense to monitor the environment before starting acoustic interactions. In comparison, fungi, lacking a visual system, rely on a cell-to-cell dialogue based on secreted signaling molecules to coordinate cell fusion and establish hyphal networks. Within this dialogue, hyphae alternate between sending and receiving signals. This pattern can be visualized via the putative signaling protein Soft (SofT), and the mitogen-activated protein kinase MAK-2 (MakB) which are recruited in an alternating oscillatory manner to the respective cytoplasmic membrane or nuclei of interacting hyphae. Here, we show that signal oscillations already occur in single hyphae of Arthrobotrys flagrans in the absence of potential fusion partners (cell monologue). They were in the same phase as growth oscillations. In contrast to the anti-phasic oscillations observed during the cell dialogue, SofT and MakB displayed synchronized oscillations in phase during the monologue. Once two fusion partners came into each other's vicinity, their oscillation frequencies slowed down (entrainment phase) and transit into anti-phasic synchronization of the two cells'; oscillations with frequencies of 104 +/- 28 sec and 117 +/- 19 sec, respectively. Single-cell oscillations, transient entrainment, and anti-phasic oscillations were reproduced by a mathematical model where nearby hyphae can absorb and secrete a limited molecular signaling component into a shared extra-cellular space. We show that intracellular Ca²⁺ concentrations oscillate in two approaching hyphae, and depletion of Ca²⁺ from the medium affected vesicle-driven extension of the hyphal tip, abolished the cell monologue and the anti-phasic synchronization of two hyphae. Our results suggest that single hyphae engage in a 'monologue' that may be used for exploration of the environment and can dynamically shift their extra-cellular signaling systems into a 'dialogue' to initiate hyphal fusion.

Data availability

All raw images and data files resulting from the analyses are available at Zenodo (https://zenodo.org/record/6830734#.Ys_KmS2w1TY).The simulation script is also available at [https://github.com/vkumpost/cell-dialog].

The following data sets were generated

1. Wernwt V
(2022) Synchronization of oscillatory growth prepares fungal hyphae for fusion
Zenodo.

https://zenodo.org/record/6830734#.Ys_KmS2w1TY

Article and author information

Author details

Valentin Wernet

Institute for Applied Biosciences, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.
Marius Kriegler

Institute for Applied Biosciences, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.
Vojtech Kumpost

Institute for Automation and Applied Informatics, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany

Competing interests
The authors declare that no competing interests exist.
Ralf Mikut

Institute for Automation and Applied Informatics, Karlsruhe Institute of Technology, Karlsruhe, Germany

Competing interests
The authors declare that no competing interests exist.
Lennart Hilbert

Institute of Biological and Chemical Systems - Biological Information Processing, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4478-5607
Reinhard Fischer

Institute for Applied Biosciences, Karlsruhe Institute of Technology, Karlsruhe, Germany

For correspondence
reinhard.fischer@kit.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6704-2569

Funding

Deutsche Forschungsgemeinschaft (Fi 459/26-1)

Reinhard Fischer

Deutsche Bundesstiftung Umwelt (2018/552)

Valentin Wernet

Helmholtz Association (HIDSS4Health)

Vojtech Kumpost
Ralf Mikut
Lennart Hilbert

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.