Molecular and morphological characterization of four new ancyromonad genera and proposal for an updated taxonomy of the Ancyromonadida

Abstract

Abstract Ancyromonads are small biflagellated protists with a bean-shaped morphology. They are cosmopolitan in marine, freshwater, and soil environments, where they attach to surfaces while feeding on bacteria. These poorly known grazers stand out by their uncertain phylogenetic position in the tree of eukaryotes, forming a deep-branching “orphan” lineage that is considered key to a better understanding of the early evolution of eukaryotes. Despite their ecological and evolutionary interest, only limited knowledge exists about their true diversity. Here, we aimed to characterize ancyromonads better by integrating environmental surveys with behavioral observation and description of cell morphology, for which sample isolation and culturing are indispensable. We studied 18 ancyromonad strains, including 14 new isolates and seven new species. We described three new and genetically divergent genera: Caraotamonas, Nyramonas, and Olneymonas, together encompassing four species. The remaining three new species belong to the already-known genera Fabomonas and Ancyromonas. We also raised Striomonas, formerly a subgenus of Nutomonas, to full genus status, on morphological and phylogenetic grounds. We studied the morphology of diverse ancyromonads under light and electron microscopy and carried out molecular phylogenetic analyses, also including 18S rRNA gene sequences from several environmental surveys. Based on these analyses, we have updated the taxonomy of Ancyromonadida.

This project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (ERC Starting Grant No 803151 to L.E. and ERC Advanced Grants No 322669 and 787904 to P.L.-G. and D.M., respectively). GT was supported by the 2019 BP 00208 Beatriu de Pinos-3 Postdoctoral Program (BP3; 801370). LG was funded by the Horizon 2020 research and innovation programme under the European Marie Skłodowska-Curie Individual Fellowship H2020-MSCA-IF-2020 (grant agreement no. 101022101 —FungEye). We are thankful for access to the Imagerie-Gif core facility at the Institute for Integrative Biology of the Cell (Gif-sur-Yvette, France) and the Electron Microscopy Facility (EMF) of the Institut de Biologie Paris-Seine (Paris, France). We thank members of the UNICELL single-cell genomics platform (https://www.deemteam.fr/en/unicell) for help in cell isolation and rRNA gene sequencing. We also thank Kaleigh Lukacs for assistance with culture maintenance.

Peer Reviewed

"Article signat per 12 autors/es: Naoji Yubuki, Guifré Torruella, Luis Javier Galindo, Aaron A. Heiss, Maria Cristina Ciobanu, Takashi Shiratori, Ken-ichiro Ishida, Jazmin Blaz, Eunsoo Kim, David Moreira, Purificación López-García, Laura Eme"

Postprint (published version)