Novel Predators Reshape Holozoan Phylogeny and Reveal the Presence of a Two-Component Signaling System in the Ancestor of Animals

Abstract

Our understanding of the origin of animals has been transformed by characterizing their most closely related, unicellular sisters: the choanoflagellates, filastereans, and ichthyosporeans. Together with animals, these lineages make up the Holozoa [1, 2]. Many traits previously considered "animal specific" were subsequently found in other holozoans [3, 4], showing that they evolved before animals, although exactly when is currently uncertain because several key relationships remain unresolved [2, 5]. Here we report the morphology and transcriptome sequencing from three novel unicellular holozoans: Pigoraptor vietnamica and Pigoraptor chileana, which are related to filastereans, and Syssomonas multiformis, which forms a new lineage with Corallochytrium in phylogenomic analyses. All three species are predatory flagellates that feed on large eukaryotic prey, and all three also appear to exhibit complex life histories with several distinct stages, including multicellular clusters. Examination of genes associated with multicellularity in animals showed that the new filastereans contain a cell-adhesion gene repertoire similar to those of other species in this group. Syssomonas multiformis possessed a smaller complement overall but does encode genes absent from the earlier-branching ichthyosporeans. Analysis of the T-box transcription factor domain showed expansion of T-box transcription factors based on combination with a non-T-box domain (a receiver domain), which has not been described outside of vertebrates. This domain and other domains we identified in all unicellular holozoans are part of the two-component signaling system that has been lost in animals, suggesting the continued use of this system in the closest relatives of animals and emphasizing the importance of studying loss of function as well as gain in major evolutionary transitions.

Novel Diversity of Deeply Branching Holomycota and Unicellular Holozoans Revealed by Metabarcoding in Middle Paraná River, Argentina

“…Regarding unicellular Holozoa, more than 60% OTUs of Paraná diversity matches with uncultured sequences, showing that the hidden diversity is still very high, especially within choanoflagellates. We also identified OTUs closely related to the newly described species Syssomonas multiformis (Hehenberger et al, 2017), which strikingly, appears to be the most abundant holozoan taxon in our dataset. Finally, we detected in our freshwater samples the presence of groups that were previously known only from marine samples; these include members of Acanthoecid choanoflagellates.…”

“…In fact, it is the richest and most abundant ichthyosporean group in the V4 region (12.9% of the total Holozoa abundance) ( Figure 4A). Surprisingly, the most abundant OTUs of all unicellular holozoans in our dataset is associated to the recently described Syssomonas multiformis, putatively the sister-group to Corallochytrium limacisporum (Hehenberger et al, 2017; Figures 5, 6). These OTUs account for 37.36% of the total unicellular Holozoa abundance in the V4 region and 45% in the V8-9 region ( Figure 4A).…”

“…Holozoa is the group that contains Metazoa and their closest unicellular relatives, namely Choanoflagellata, Filasterea, Ichthyosporea, and Plurimorfea, the latter with an uncertain phylogenetic position in relation to Ichthyosporea (Paps and Ruiz-Trillo, 2010;Torruella et al, 2015;Hehenberger et al, 2017). Holozoa also contains some exclusively environmental clades, mainly within choanoflagellates and ichthyosporeans (del Campo and Ruiz-Trillo, 2013).…”

“…The majority of these environmental lineages of opisthokonts were described in marine environments. However, a few new species have been recently described in fresh waters; these include the genera Syssomonas and Pigoraptor (Hehenberger et al, 2017) within Holozoa and Parvularia as an early-branching Holomycota (López-Escardó et al, 2018). Therefore, there is need for exploring the diversity of unicellular opisthokonts, particularly from freshwater environments where a wide range of ecological niches exist (Logares et al, 2009a;Simon et al, 2015).…”

“…Holozoa contains animals and their unicellular relatives, namely Choanoflagellata, Filasterea and Teretosporea (or Ichthyosporea and Plurimorfea, depending on the authors) (Lang et al, 2002;Torruella et al, 2012Torruella et al, , 2015Hehenberger et al, 2017). Holomycota contains fungi and their closest unicellular lineages (Brown et al, 2009;Liu et al, 2009;Lara et al, 2010;López-Escardó et al, 2018).…”