Data from Chytrid rhizoid morphogenesis resembles hyphal development in multicellular fungi and is adaptive to resource availability

Key to the ecological prominence of fungi is their distinctive cell biology, our understanding of which has been principally based on dikaryan hyphal and yeast forms. The early-diverging Chytridiomycota (chytrids) are ecologically important and a significant component of fungal diversity, yet their cell biology remains poorly understood. Unlike dikaryan hyphae, chytrids typically attach to substrates and feed osmotrophically via anucleate rhizoids. The evolution of fungal hyphae appears to have occurred from rhizoid-bearing lineages and it has been hypothesized that a rhizoid-like structure was the precursor to multicellular hyphae. Here, we show in a unicellular chytrid, <i>Rhizoclosmatium globosum</i>, that rhizoid development exhibits striking similarities with dikaryan hyphae and is adaptive to resource availability. Rhizoid morphogenesis exhibits analogous patterns to hyphal growth and is controlled by β-glucan-dependent cell wall synthesis and actin polymerisation. Chytrid rhizoids growing from individual cells also demonstrate adaptive morphological plasticity in response to resource availability, developing a searching phenotype when carbon starved and spatial differentiation when interacting with particulate organic matter. We demonstrate that the adaptive cell biology and associated developmental plasticity considered characteristic of hyphal fungi are shared more widely across the Kingdom Fungi and therefore could be conserved from their most recent common ancestor.

真菌在生态系统中的核心地位源于其独特的细胞生物学特性，目前我们对该特性的认知主要基于双核（dikaryan）菌丝与酵母形态类群。早期分化的壶菌门（Chytridiomycota，俗称壶菌chytrids）是生态系统中的重要类群，也是真菌多样性的重要组成部分，但其细胞生物学机制仍鲜为人知。与双核真菌的菌丝不同，壶菌通常附着于基质，并通过无核假根（rhizoids）以渗透营养方式获取营养。真菌菌丝的演化被认为起源于具有假根的类群，且有假说提出，类似假根的结构是多细胞菌丝的前体。本研究针对单细胞壶菌<i>Rhizoclosmatium globosum</i>展开研究，发现其假根的发育与双核真菌的菌丝具有显著相似性，且该发育过程可响应资源可获得性产生适应性调整。假根的形态发生过程与菌丝生长模式类似，受β-葡聚糖（β-glucan）依赖的细胞壁合成以及肌动蛋白聚合（actin polymerisation）调控。从单个细胞长出的壶菌假根，还可响应资源可获得性表现出适应性形态可塑性：在碳源匮乏时形成搜索型表型，而在与颗粒有机物（particulate organic matter）互作时则呈现空间分化特征。本研究证实，此前被认为是菌丝状真菌特有的适应性细胞生物学特性及相关发育可塑性，在真菌界中分布更为广泛，因此该特征可能起源于真菌的最近共同祖先（most recent common ancestor）。