Hidden diversity in the oomycete genus Olpidiopsis is a potential hazard to red algal cultivation and conservation worldwide

Marine species of the oomycete genus Olpidiopsis that infect cultivated red macroalgae, most notably Pyropia spp., are one of the main causes of economic loss in the Asian seaweed industry. We recently described novel Olpidiopsis species infecting red algae in Scotland, and thus hypothesized that this genus is more abundant and widespread than previously recognized. Here, we show that the eukaryotic microbiome of macroscopically healthy Porphyra umbilicalis thalli frequently contains marker genes closely related to Olpidiopsis. Thanks to a custom pipeline that allows for de novo OTU and biogeography discovery, and the recovery of precomputed OTUs from large-scale metabarcoding campaigns, we unveil more than 20 unknown Olpidiopsis taxa with a worldwide distribution. Additionally, laboratory-controlled cross-infection experiments show that a Scottish variety of O. porphyrae is virulent on the most commonly cultivated Pyropia yezoensis cultivar in Korea and that conversely, a Korean strain of O. porphyrae successfully infects wild Bangia sp. strains isolated from Scotland. These results provide proof-of-concept that a native Olpidiopsis pathogen may threaten an introduced crop or that an Olpidiopsis pathogen potentially introduced alongside a non-native crop might cross-infect a native European alga. Thus, we draw parallels with several current biosecurity crises, where major risks to native floras and faunas, as well as crops, are caused by the inadvertent introduction of poorly known pathogens through the agricultural and horticultural trades. Therefore, we express concern that the rapid growth of algal cultivation worldwide, linked to international movement of seaweed seed and the absence of biosecurity monitoring or regulation pertaining to this trade, potentially lays the ground for grave ecological and economic crises in the marine environment.