A re-evaluation of the Paraphysoderma sedebokerense life cycle, evidence of spore aggregation during infection, and their implications for the management of blastocladialean pathogens of algae and plant crops

The blastocladialean fungus Paraphysoderma sedebokerense is a devastating pathogen of unicellular green algae, that hinders their commercial cultivation. It is sister to Physoderma, a genus encompassing pathogens of ferns and angiosperms that causes major crop losses on Fabaceae and maize. Depending on favourable or unfavourable growth conditions, P. sedebokerense switches between vegetative, thin-walled cysts and resting, thick-walled cysts. Here, we identify P. sedebokerense novel life stages, including endobiotic structures inside algal host cells, yellow propagules and multiflagellated zoospores. This led us to reevaluate its life cycle and hypothesize the existence of facultative gametes developing parthenogenetically in the absence of fertilisation. Via the investigation of P. sedebokerense development without its host, we unveil that parthenogenetic, saprotrophic development occurs during the epibiotic life stage. Finally, we show that there is aggregation of P. sedebokerense propagules on the algal host cells and validate a low-cost, high-throughput cell-classification method to quantify this non-random spatial distribution at low prevalence of infection. In the future, identifying ways to disrupt aggregation would block infection at the earliest stages of an outbreak, providing algal farmers with an efficient route to manage this pathogen. We also provide evidence that the life cycle of P. sedebokerense much more closely resembles the life cycle of Physoderma spp. than previously thought; this implies that Paraphysoderma (and the protocols developed here) might be used as a convenient in vitro model to test the efficacy of treatments against devastating Physoderma pathogens.