The Chytrid-like Parasites of Algae Amoeboradix gromovi gen. et sp. nov. and Sanchytrium tribonematis Belong to a New Fungal Lineage

Abstract

Fungi encompass, in addition to classically well-studied lineages, an ever-expanding diversity of poorly known lineages including zoosporic chytrid-like parasites. Here, we formally describe Amoeboradix gromovi gen. et sp. nov. comprising a set of closely related strains of chytrid-like parasites of the yellow-green alga Tribonema gayanum unusually endowed with amoeboid zoospores. Morphological and ultrastructural features of A. gromovi observed by light and transmission electron microscopy recall previous descriptions of Rhizophydium anatropum. A. gromovi exhibits one of the longest kinetosomes known in eukaryotes, composed of microtubular singlets or doublets. To carry out molecular phylogenetic analysis and validate the identification of different life cycle stages, we amplified 18S rRNA genes from three A. gromovi strains infecting T. gayanum cultures, single sporangia and single zoospores. Molecular phylogenetic analyses of 18S+28S rRNA concatenated genes of the type strain revealed that A. gromovi is closely related to the recently described species Sanchytrium tribonematis, another parasite of Tribonema that had been tentatively classified within Monoblepharidomycetes. However, our phylogenetic analysis with an extended taxon sampling did not show any particular affinity of Amoeboradix and Sanchytrium with described fungal taxa. Therefore, Amoeboradix gromovi and Sanchytrium tribonematis likely represent a new divergent taxon that remains incertae sedis within Fungi.

The Ultrastructure of Sanchytrium tribonematis (Sanchytriaceae, Fungi incertae sedis) Confirms its Close Relationship to Amoeboradix

“…Recently, we obtained 18S and 28S rRNA gene data for Amoeboradix gromovi, a chytrid-like fungus having peculiar traits and resembling the classical Rhizophydium anatropum. Surprisingly, phylogenetic analyses of these two markers showed that Amoeboradix formed a tight cluster with another chytrid-like organism, Sanchytrium tribonematis, branching in a basal position to the Glomeromycota and Dikarya cluster, albeit with low support (Karpov et al 2018). The Amoeboradix-Sanchytrium clade is very divergent and represents a new fungal lineage.…”

“…Surprisingly, phylogenetic analyses of these two markers showed that Amoeboradix formed a tight cluster with another chytrid‐like organism, Sanchytrium tribonematis, branching in a basal position to the Glomeromycota and Dikarya cluster, albeit with low support (Karpov et al. ). The Amoeboradix‐Sanchytrium clade is very divergent and represents a new fungal lineage.…”

“…Amoeboradix possesses rather peculiar ultrastructural features, notably its amoeboid zoospores contain an extremely long (2 μm) and at the same time reduced kinetosome composed of singlets/doublets (not triplets) of microtubules (Karpov et al. ).…”

“…However, so far only A. gromovi has been characterized morphologically and ultrastructurally, and it is therefore not possible to define synapomorphies for the family Sanchytriaceae. Amoeboradix possesses rather peculiar ultrastructural features, notably its amoeboid zoospores contain an extremely long (2 lm) and at the same time reduced kinetosome composed of singlets/doublets (not triplets) of microtubules (Karpov et al 2018).…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…Consistent with an ancient origin of all three phenotypes, amoeboid, flagellate and amoeboflagellate cells are all broadly distributed in opisthokonts (animals, fungi, and their relatives). Interestingly, amoeboflagellate phenotypes have recently been described in several species occupying key phylogenetic positions, including in the sister-group of choanozoans (the filastereans) 37,38 , in early-branching fungi 39,68,69 , in the two closest known relatives of opisthokonts (apusomonads 70 and breviates 71 ), and in early-branching amoebozoans 72 . This is consistent with an ancient origin and broad conservation of the amoeboflagellate phenotype in opisthokonts 73 .…”