Karlsruhe Institute of Technology - South Campus Institute for Applied Biosciences Dept. of Microbiology, Karlsruhe, Germany.
Karlsruhe Institute of Technology - North Campus Institute for Automation and Applied Informatics, Eggenstein-Leopoldshafen, Germany.
Elife. 2023 Aug 21;12:e83310. doi: 10.7554/eLife.83310.
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 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 s and 117±19 s, 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 extracellular space. We show that intracellular Ca concentrations oscillate in two approaching hyphae, and depletion of Ca 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 extracellular signaling systems into a 'dialogue' to initiate hyphal fusion.
沟通对于生物有机相互作用至关重要，从细菌、真菌到人类都是如此。人类可能会在开始声学相互作用之前使用视觉来监测环境。相比之下，真菌缺乏视觉系统，依赖于基于分泌信号分子的细胞间对话来协调细胞融合并建立菌丝网络。在这种对话中，菌丝交替发送和接收信号。这种模式可以通过假定的信号蛋白 Soft（SofT）和丝裂原激活蛋白激酶 MAK-2（MakB）来可视化，它们以交替的振荡方式被招募到相互作用的菌丝的细胞质膜或核中。在这里，我们表明，在没有潜在融合伙伴的情况下（细胞独白），单个菌丝中已经存在信号振荡。它们与生长振荡处于同一相位。与细胞对话中观察到的反相振荡相反，SofT 和 MakB 在独白过程中相位同步振荡。一旦两个融合伙伴彼此靠近，它们的振荡频率就会减慢（同步相位），并转变为两个细胞的振荡反相同步，频率分别为 104±28 s 和 117±19 s。单细胞振荡、瞬时同步和反相同步通过一个数学模型得到再现，其中附近的菌丝可以将有限的分子信号成分吸收并分泌到共享的细胞外空间中。我们表明，在两个接近的菌丝中细胞内 Ca 浓度振荡，并且从中介质中耗尽 Ca 会影响菌丝尖端的囊泡驱动延伸，从而破坏细胞独白和两个菌丝的反相同步。我们的结果表明，单个菌丝参与“独白”，可能用于环境探索，并可以将其细胞外信号系统动态切换到“对话”以启动菌丝融合。
