A cellular and molecular atlas reveals the basis of chytrid development

Abstract

The chytrids (phylum Chytridiomycota) are a major fungal lineage of ecological and evolutionary importance. Despite their importance, many fundamental aspects of chytrid developmental and cell biology remain poorly understood. To address these knowledge gaps, we combined quantitative volume electron microscopy and comparative transcriptome profiling to create an ‘atlas’ of the cellular and molecular basis of the chytrid life cycle, using the model chytrid Rhizoclosmatium globosum. From our developmental atlas, we describe the transition from the transcriptionally inactive free-swimming zoospore to the more biologically complex germling, and show that lipid processing is multifaceted and dynamic throughout the life cycle. We demonstrate that the chytrid apophysis is a compartmentalised site of high intracellular trafficking, linking the feeding/attaching rhizoids to the reproductive zoosporangium, and constituting division of labour in the chytrid cell plan. We provide evidence that during zoosporogenesis, zoospores display amoeboid morphologies and exhibit endocytotic cargo transport from the interstitial maternal cytoplasm. Taken together, our results reveal insights into chytrid developmental biology and provide a basis for future investigations into non-dikaryan fungal cell biology.

Evolutionary and biological mechanisms underpinning chitin degradation in aquatic fungi

“…The biological mechanisms underpinning chemotaxis in aquatic chytrids are poorly understood (Laundon and Cunliffe 2021). It is possible that response to environmental signals could be linked to the rumposome, an enigmatic structure connecting the zoospore cell surface to the flagellar machinery that is present in R. globosum JEL800 zoospores (Laundon et al 2022) and is likely a site of calcium-mediated signalling (Powell 1983). Phototaxis has also been shown in chytrid zoospores, including with R. globosum JEL800, facilitated by a CyclOp-fusion protein based sensory system (Galindo et al 2022).…”

“…encystment) is a possible trait that could facilitate the rapid colonisation and exploitation of ephemeral chitin-rich substrates such as mayfly exuviae in a dynamic resource-complex and competitive environment. Chytrid zoospore biology is poorly understood, including controls on the cell cycle (Medina and Buchler 2020, Laundon et al 2022), however based on frog mucus exposure experiments with B. dendrobatidis , likely involve critical host/substrate chemical cues that initiate encystment via calcium signalling and actin cytoskeleton remodelling (Robinson et al 2022). Chytrid zoospores are metabolically active, yet are transcriptionally and translationally inactive, with ribosomes held dormant (Medina and Buchler 2020).…”

“…Rhizoclosmatium globosum is an aquatic chytrid found prevalent in nature attached to chitin-rich arthropod exuviae (Sparrow 1960). The strain R. globosum JEL800 is an emerging model for biological and evolutionary studies of early diverging fungi (Laundon et al 2020, Venard et al 2020, Prostak et al 2021, Galindo et al 2022, Laundon et al 2022) that was isolated by chitin baiting (Joyce Longcore, pers. comm.)…”

Genomes and transcriptomes help unravel the complex life cycle of the blastoclad fungus,Coelomomyces lativittatus,an obligate parasite of mosquitoes and microcrustaceans

“…al . posited that the chytrid zoospore life stage is optimized for dispersal to new hosts rather than general metabolism [90]. The authors also reported complex lipid dynamics throughout the lifecycle of the chytrid, Rhizoclosmatium globosum .…”

Functional diversity of microbial eukaryotes in a meromictic lake: Coupling between metatranscriptomic and a trait‐based approach

“…Those of the large size fractions over‐express genes which may be likely involved in attached lifestyle during which they have to degrade the hosts' cell wall and hijack its lipid reserves (Gerphagnon et al, 2019). On the contrary, those of the small size fraction over‐express genes involved in glycolipids anabolisms, which have recently been described to take place during zoospore germination by Laundon et al (2022). Finally, some groups do not seem to be affected by size fraction such as saprotrophs for which neither taxonomic diversity nor metabolic potential variations are detected.…”