Nuclear dynamics in a fungal chimera

Abstract

A fungal colony is a syncytium composed of a branched and interconnected network of cells. Chimerism endows colonies with increased virulence and ability to exploit nutritionally complex substrates. Moreover, chimera formation may be a driver for diversification at the species level by allowing lateral gene transfer between strains that are too distantly related to hybridize sexually. However, the processes by which genomic diversity develops and is maintained within a single colony are little understood. In particular, both theory and experiments show that genetically diverse colonies may be unstable and spontaneously segregate into genetically homogenous sectors. By directly measuring patterns of nuclear movement in the model ascomycete fungus Neurospora crassa, we show that genetic diversity is maintained by complex mixing flows of nuclei at all length scales within the hyphal network. Mathematical modeling and experiments in a morphological mutant reveal some of the exquisite hydraulic engineering necessary to create the mixing flows. In addition to illuminating multinucleate and multigenomic lifestyles, the adaptation of a hyphal network for mixing nuclear material provides a previously unexamined organizing principle for understanding morphological diversity in the more-thana-million species of filamentous fungi.heterokaryon | hydrodynamics | biological networks G enetic diversity between individuals is important to the resilience of species (1) and ecosystems (2). However, physical and genetic barriers constrain internal genetic diversity within single organisms: Cell walls limit nuclear movement between cells, whereas separation of germ and somatic cell lines means that diversity created by somatic mutations is not transmitted intergenerationally. However, in syncytial organisms, including filamentous fungi and plasmodial slime molds (3), populations of genetically different and mobile nuclei may share a common cytoplasm ( Fig. 1A and Movie S1). Internal diversity may be acquired by accumulation of mutations as the organism grows or by somatic fusion followed by genetic transfer between individuals. For filamentous fungi, intraorganismic diversity is ubiquitous (4, 5). Shifting nuclear ratios to suit changing or heterogeneous environments enhances growth on complex substrates such as plant cell walls (6) and increases fungal virulence (7). Fusion between different fungal individuals is limited by somatic (heterokaryon) compatibility barriers (8), and most internal genetic diversity results from mutations within a single, initially homokaryotic individual (4). However, somatic compatibility barriers are not absolute (9), and exchange of nuclei between heterospecific individuals is now believed to be a motor for fungal diversification (10-12).A fungal chimera must maintain its genetic richness during growth. Maintenance of richness is challenging because fungal mycelia, which are made up of a network of filamentous cells (hyphae), grow by extension of hyphal tips. A continual tipward flow of vesicles and n...

Chemotropism and Cell Fusion in Neurospora crassa Relies on the Formation of Distinct Protein Complexes by HAM-5 and a Novel Protein HAM-14

“…In fungi, vegetative fusion enables a fungal colony to share resources and has implications for fitness and virulence (Craven et al 2008;Fricker et al 2009;Eaton et al 2011;Richard et al 2012;Simonin et al 2012;Roper et al 2013;Chagnon 2014). In the filamentous ascomycete fungus, Neurospora crassa, genetically identical germinated asexual spores (germlings) undergo fusion to form a syncytium that is an interconnected network of fused cells Leeder et al 2013;Herzog et al 2015).…”

“…We predict that the function of both HAM-5 and HAM-14 in fusion and colony development will be conserved in a wide range of filamentous ascomycete fungi. Cell fusion and the ability to form a syncytium provides a fungal colony with many advantages ranging from improved fitness and enhanced ability to adapt to the environment, in addition to mixing of genetic material and cellular components (Richard et al 2012;Roper et al 2013;Bastiaans et al 2015). Also, for some plant pathogenic fungi, the ability to fuse affects the ability to form an infection network or is a prerequisite to infect their host (Craven et al 2008;Prados Rosales and Di Pietro 2008;Guo et al 2015).…”

Maintaining Two Mating Types: Structure of the Mating Type Locus and Its Role in Heterokaryosis inPodospora anserina

“…No such cellular mechanism faithfully maintaining heterokaryosis in mycelia is known in Ascomycota (while one exists in the sexual lineage). In the absence of nuclear mixing, mathematical modeling showed that heterokaryotic thalli should often break down into homokaryons (Roper et al 2013). Pseudohomothallic Ascomycota, such as Podospora anserina and Neurospora tetrasperma, produce mat+/mat2 (or mat A/mat a) dikaryotic ascospores, which upon germination yield a self-fertile heterokaryotic mycelium (Raju and Perkins 1994).…”

Early Colony Establishment in Neurospora crassa Requires a MAP Kinase Regulatory Network

“…Cell fusion between genetically identical cells can be mediated by cells that have differentiated, but in some cases, also between cells in an identical developmental state, for example, cell fusion between germinating asexual spores (conidia) of filamentous fungi (Pandey et al 2004;Roca et al 2005a;Read et al 2010). In filamentous fungi, these fusions are integral to the formation of an interconnected hyphal network, which mediates genetic mixing and the sharing of resources (Simonin et al 2012;Roper et al 2013). How this process is initiated and maintained and what proteins are involved are still mostly unknown.…”