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

Davis Laundon,Michael Cunliffe,Nathan Chrismas,Glen Wheeler

doi:10.1098/rspb.2020.0433

Abstract

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, Rhizoclosmatium globosum, 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 polymerization. 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.

Highlights

Hyphae are polarized, elongating and bifurcating cellular structures that many fungi use to forage and feed
The improved understanding of chytrid rhizoid biology related to substrate attachment and feeding we present here opens the door to a greater insight into the functional ecology of chytrids and their environmental potency
Our approach of combining live cell confocal microscopy with three-dimensional rhizoid reconstruction provides a powerful toolkit for morphometric quantification of chytrid cell development and could shed light on the biology underpinning chytrid ecological prevalence

Summary

Introduction

Hyphae are polarized, elongating and bifurcating cellular structures that many fungi use to forage and feed (figure 1a and b). Chytrids produce filamentous hyphae-like, anucleate structures called rhizoids (figure 1a–c) [3], which are important in their ecological functions, in terms of both attachment to substrates and osmotrophic feeding [2]. Given the importance of rhizoids in both contemporary and paleo-chytrid ecology, there remains a limited understanding of chytrid rhizoid biology, including possible similarities with functionally analogous hyphae in other fungi and the potential for substrate-dependent adaptations. Character mapping of the presence of cellular growth plans against established phylogenies reveals the multicellular hyphal form to be a derived condition, whereas rhizoid feeding structures are the basal condition within the true fungi royalsocietypublishing.org/journal/rspb Proc. B 287: 20200433 length of the rhizoidal growth unit (μm, log scale)

Methods

Discussion

Conclusion