Expanding the molecular and morphological diversity of Apusomonadida, a deep-branching group of gliding bacterivorous protists

Apusomonads are cosmopolitan bacterivorous biflagellate protists usually gliding on freshwater and marine sediment or wet soils. These nanoflagellates form a sister lineage to opisthokonts and may have retained ancestral features helpful to understanding the early evolution of this large supergroup. Although molecular environmental analyses indicate that apusomonads are genetically diverse, few species have been described. Here, we morphologically characterize 11 new apusomonad strains. Based on molecular phylogenetic analyses of the rRNA gene operon, we describe four new strains of the known species Multimonas media, Podomonas capensis, Apusomonas proboscidea, and Apusomonas australiensis, and rename Thecamonas oxoniensis as Mylnikovia oxoniensis n. gen., n. comb. Additionally, we describe four new genera and six new species: Catacumbia lutetiensis n. gen. n. sp., Cavaliersmithia chaoae n. gen. n. sp., Singekia montserratensis n. gen. n. sp., Singekia franciliensis n. gen. n. sp., Karpovia croatica n. gen. n. sp., and Chelonemonas dolani n. sp. Our comparative analysis suggests that apusomonad ancestor was a fusiform biflagellate with a dorsal pellicle, a plastic ventral surface, and a sleeve covering the anterior flagellum, that thrived in marine, possibly oxygen-poor, environments. It likely had a complex cell cycle with dormant and multiple fission stages, and sex. Our results extend known apusomonad diversity, allow updating their taxonomy, and provide elements to understand early eukaryotic evolution.
The authors acknowledge the importance of previous studies on these protists by several researchers and thank T. Cavalier-Smith, E. Chao, D. Patterson, A. Mylnikov, and S. A. Karpov for their legacy and, in specific cases, useful discussion and collaboration. We thank J. Dolan for access to samples from Villefranche-sur-Mer from which C. dolani was cultured, A. Guillén, author of ‘Proyecto agua’, for sending samples from the Sanabria glacial lake, and J. Favate for collecting the material from which SPRINTER was isolated. We also thank Kaleigh Lukacs for assisting with culture maintenance. This work was supported by the European Research Council (ERC) Advanced Grants ‘Protistworld’ and ‘Plast‐Evol’ (322669 and 787904, respectively) the Horizon 2020 research and innovation program under the Marie Skłodowska-Curie ITN project SINGEK H2020-MSCA-ITN-2015-675752 (http://www.singek.eu/). GT was supported by the 2019 BP 00208 Beatriu de Pinos-3 Postdoctoral Program (BP3; 801370)
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