Marinomyxa Gen. Nov. Accommodates Gall-Forming Parasites of the Tropical to Subtropical Seagrass Genus Halophila and Con

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Marinomyxa Gen. Nov. Accommodates Gall-Forming Parasites of the Tropical to Subtropical Seagrass Genus Halophila and Constitutes a Novel Deep-Branching Lineage Within Phytomyxea (Rhizaria: Endomyxa) Viktorie Kolátková 1

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Ivan Čepička 2 & Razy Hoffman 3 & Martin Vohník 4,5

Received: 11 July 2020 / Accepted: 28 September 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Marine representatives of Phytomyxea (SAR: Rhizaria: Endomyxa), a peculiar class of obligate endobiotic parasites, are a greatly understudied ecological group of protists infecting many algal, diatom, and seagrass species. Very little is known about the actual diversity, ecology, and pathogenic potential of these organisms and their taxonomic treatment in many cases follows outdated morphotaxonomic concepts. Here we focused on resolving the phylogenetic relations of the phytomyxean parasites of the widespread seagrass genus Halophila. We report the first finding of Plasmodiophora halophilae, the parasite of ovate-leaf Halophila species, after more than 100 years since its original description in 1913. We provide additional information on its anatomy, morphology, distribution, and host range, together with a phylogenetic evidence that it is congeneric with the recently rediscovered species infecting the invasive seagrass Halophila stipulacea in the Mediterranean Sea. Despite the previously hypothesized affiliation of the latter to Tetramyxa, our phylogenetic analyses of the 18S rRNA gene place Tetramyxa parasitica (a parasite of brackish water phanerogams and the type species of the genus) in the freshwater/terrestrial phytomyxean order Plasmodiophorida and reveal that phytomyxids associated with Halophila spp. form a separate deep-branching clade within the class proposed here as Marinomyxa gen. nov. We further argue that M. marina infecting H. stipulacea is most likely a speciesspecific parasite and implies their comigration through the Suez Canal. Keywords Seagrass symbionts . Phytomyxids . TAGIRI-5 . 18S rRNA phylogeny . Plasmodiophora halophilae . Tetramyxa marina

Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01615-5) contains supplementary material, which is available to authorized users. * Viktorie Kolátková [email protected] 1

Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic

2

Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

3

The Steinhardt Museum of Natural History and Israel National Center for Biodiversity Studies, Tel Aviv University, Tel Aviv, Israel

4

Department of Mycorrhizal Symbioses, Institute of Botany, Czech Academy of Sciences, Průhonice, Czech Republic

5

Department of Experimental Plant Biology, Faculty of Science, Charles University, Prague, Czech Republic

Introduction The continuing boom of environmental sequencing and metagenomics has uncovered an immense microbial diversity both in water and soil, reaching far b