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Viruses, bacteria, and eukaryotic symbionts interact with algae in a variety of ways to cause disease complexes, often shaping marine and freshwater ecosystems. The advent of phyconomy (a.k.a. seaweed agronomy) represents a need for a greater understanding of algal disease interactions, where underestimated cryptic diversity and lack of phycopathological basis are prospective constraints for algal domestication. Here, we highlight the limited yet increasing knowledge of algal pathogen biodiversity and the ecological interaction with their algal hosts. Finally, we discuss how ecology and cultivation experience contribute to and reinforce aquaculture practice, with the potential to reshape biosecurity policies of seaweed cultivation worldwide. Expected final online publication date for the Annual Review of Phytopathology, Volume 61 is September 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

SummaryPhagocytosis is a complex multi-gene trait of eukaryotes and allegedly one of the very defining features of this group. Although well documented for free-living unicellular eukaryotes and in specific cellular types of animals, data on phagocytosis in intracellular biotrophic parasites are scant. Indeed, the definition of intracellular biotrophy as complete reliance of a parasite on a living host, with which it constantly negotiates for the exchange of nutrients, is at odd with the consumption of particulate matter suggested by phagocytosis. Phytomyxea are intracellular biotrophic parasites infecting a broad group of hosts, ranging from plants to stramenopiles. They belong to the clade Rhizaria, where phagotrophy (i.e., phagocytosis as main mode to acquire nutrients) is the main mode of nutrition. The exact mode of nutrition of the biotrophic phytomyxea, including the agriculturally impactful phytomyxid Plasmodiophora brassicae, is still unresolved; despite investigations and the availability of molecular data. For other Phytomyxea, observations are patchy and molecular data altogether lacking. Here, using available genomic and transcriptomic data for Phytomyxea and the de novo sequenced transcriptome of the brown algae parasite Maullinia ectocarpii, we investigate the likelihood that the genetic machinery underpinning phagotrophy is conserved within the clade. We further document intracellular phagocytosis in P. brassicae and M. ectocarpii by transmission electron microscopy and fluorescent in situ hybridization. Our investigations confirm that molecular signatures underpinning phagocytosis exist in Phytomyxea and hint at a smaller subset of genes used for intracellular phagocytosis, which is similar between the two parasites. Microscopic evidence confirms the existence of intracellular phagocytosis, which seems to coexist with the manipulation of host physiology typical of biotrophic interactions. In both phytomyxid parasites investigated intracellular phagocytosis has adapted to the intracellular environment and seemingly targets specific organelles. Our findings shed light on the feeding behaviour of Phytomyxea, providing new molecular data for the class; and suggest a paramount and previously unrecognised role for phagocytosis in biotrophic interactions between host and parasite.

This study reports the first record of Sorosphaerula radicalis (Phytomyxea, Rhizaria) in continental Europe (Tirol, Austria) and provides first molecular data for this species. An 18S rRNA phylogeny placed S. radicalis into the Plasmodiophorida, although distant from other members of the genus Sorosphaerula and close to the parasite of water cress Hillenburgia nasturtii. To resolve this polyphyly, we compare morphological data and life cycles of Sorosphaerula veronicae (the type species of the genus Sorosphaerula), Hillenburgia nasturtii, and Sorosphaerula radicalis. We conclude that Sorosphaerula radicalis belongs to the recently established genus Hillenburgia.

Chytrids have long been recognised as important parasites of microalgae in freshwater systems, able to shape the dynamics of blooms, the gene pool of their host and phytoplankton succession. In the sea however, where the presence of these organisms is erratic and ephemeral, studies concerning chytrids are sparse and confined to metabarcoding surveys or microscopy observations. Despite the scarcity of data, chytrid epidemics are supposed to play an important role in marine biogeochemical cycles, being one of the drivers of phytoplankton dynamics. Here we combine microscopy observations and in silico mining of a single-cell whole genome to molecularly and morphologically characterise a novel chytrid parasite of the dominant diatom genus Skeletonema. Morphological observations highlight features of the thallus and ascertain the parasitic nature of the interaction whilst the genetic markers obtained allows for a phylogenetic reconstruction, placing the new species in the order Rhizophydiales. Thanks to the molecular data obtained we are also able to provide a first investigation of the global distribution of this organism by screening the Ocean Sampling Day (OSD) dataset, highlighting a northern transatlantic dissemination.

Parasites are key drivers of phytoplankton bloom dynamics and related aquatic ecosystem processes. Yet, the dearth of morphological and molecular information hinders the assessment of their diversity and ecological role. Using single-cell techniques, we characterise morphologically and molecularly, intracellular parasitoids infecting four potentially toxin-producing Pseudo-nitzschia and one Melosira species on the North Atlantic coast. These sequences define two, morphologically indistinguishable clades within the phylum Oomycota, related to the genera of algal parasites Anisolpidium and Olpidiopsis and the diatom parasitoid species Miracula helgolandica. Our morphological data are insufficient to attribute either clade to the still unsequenced genus Ectrogella; hence it is proposed to name the clades OOM_1 and OOM_2. A screening of global databases of the barcode regions V4 and V9 of the 18S rDNA demonstrate the presence of these parasitoids beyond the North Atlantic coastal region. During a biweekly metabarcoding survey (Concarneau Bay, France), reads associated with one sequenced parasitoid coincided with the decline of Cerataulina pelagica bloom, whilst the other parasitoids co-occurred at low abundance with Pseudo-nitzschia. Our data highlight a complex and unexplored diversity of the oomycete parasitoids of diatoms and calls for the investigation of their phenology, evolution, and potential contribution in controlling their host spatial-temporal dynamics.

Parasitic Chytridiomycota (chytrids) are ecologically significant in various aquatic ecosystems, notably through their roles in controlling bloom-forming phytoplankton populations and in facilitating the transfer of nutrients from inedible algae to higher trophic levels. The diversity and study of these obligate parasites, while critical to understand the interactions between pathogens and their hosts in the environment, have been hindered by challenges inherent to their isolation and stable long-term maintenance under laboratory conditions. Here, we isolated an obligate chytrid parasite (CCAP 4086/1) on the freshwater bloom-forming diatom Asterionella formosa and characterized its infectious cycle under controlled conditions. Phylogenetic analyses based on 18S, 5.8S, and 28S ribosomal DNAs (rDNAs) revealed that this strain belongs to the recently described clade SW-I within the Lobulomycetales. All morphological features observed agree with the description of the known Asterionella parasite Zygorhizidium affluens Canter. We thus provide a phylogenetic placement for this chytrid and present a robust and simple assay that assesses both the infection success and the viability of the host. We also validate a cryopreservation method for stable and cost-effective long-term storage and demonstrate its recovery after thawing. All the above-mentioned tools establish a new gold standard for the isolation and long-term preservation of parasitic aquatic chytrids, thus opening new perspectives to investigate the diversity of these organisms and their physiology in a controlled laboratory environment. IMPORTANCE Despite their ecological relevance, parasitic aquatic chytrids are understudied, especially due to the challenges associated with their isolation and maintenance in culture. Here we isolated and established a culture of a chytrid parasite infecting the bloom-forming freshwater diatom Asterionella formosa. The chytrid morphology suggests that it corresponds to the Asterionella parasite known as Zygorhizidium affluens. The phylogenetic reconstruction in the present study supports the hypothesis that our Z. affluens isolate belongs to the order Lobulomycetales and clusters within the novel clade SW-I. We also validate a cryopreservation method for stable and cost-effective long-term storage of parasitic chytrids of phytoplankton. The establishment of a monoclonal pathosystem in culture and its successful cryopreservation opens the way to further investigate this ecologically relevant parasitic interaction.

The rapid growth of marine macroalgal cultivation amplifies the potential impacts of seaweed diseases. Here, we combine microscopy and molecular analysis to describe two novel European species, Olpidiopsis palmariae and O. muelleri spp. nov., that infect the commercially important red algae Palmaria and Porphyra, respectively. A Scottish variety of Olpidiopsis porphyrae, a devastating pathogen of Pyropia previously thought to be restricted to Japanese seaweed farms, is also described as O. porphyrae var. scotiae. In the light of their destructiveness in Asian farms, together with the global expansion of algal cultivation and pertaining seed trade, Olpidiopsis pathogens should be treated as a serious threat to the sustainability of red algal aquaculture. Our findings call for the documentation of seaweed pathogens and the creation of an international biosecurity framework to limit their spread.

The diatom genera Licmophora and Fragilaria are frequent epiphytes on marine macroalgae and can be infected by intracellular parasitoids traditionally assigned to the oomycete genus Ectrogella. Much debate and uncertainty remains about the taxonomy of these oomycetes, not least due to their morphological and developmental plasticity. Here, we used single-cell techniques to obtain partial sequences of the parasitoids 18S and cox2 genes. The former falls into two recently identified clades of Pseudo-nitzschia parasites temporarily named OOM_1_2 and OOM_2, closely related to the genera of brown and red algal pathogens Anisolpidium and Olpidiopsis. A third group of sequences falls at the base of the red algal parasites assigned to Olpidiopsis. In one instance, two oomycete parasitoids seemed to co-exist in a single diatom cell; this co-occurrence of distinct parasitoid taxa not only within a population of diatom epiphytes, but also within the same host cell, possibly explains the ongoing confusion in the taxonomy of these parasitoids. We demonstrate the polyphyly of Licmophora parasitoids previously assigned to Ectrogella (sensu Sparrow, 1960) and show that parasites of red algae assigned to the genus Olpidiopsis are most likely not monophyletic. We conclude that combining single-cell microscopy and molecular methods is necessary for their full characterisation.