Gene Similarity Networks Unveil a Potential Novel Unicellular Group Closely Related to Animals from the Tara Oceans Expedition

Abstract

The Holozoa clade comprises animals and several unicellular lineages (choanoflagellates, filastereans and teretosporeans). Understanding their full diversity is essential to address the origins of animals and other evolutionary questions. However, they are poorly known. To provide more insights into the real diversity of holozoans and check for undiscovered diversity, we here analysed 18S rDNA metabarcoding data from the global Tara Oceans expedition. To overcome the low phylogenetic information contained in the metabarcoding dataset (composed of sequences from the short V9 region of the gene), we used similarity networks by combining two datasets: unknown environmental sequences from Tara Oceans and known reference sequences from GenBank. We then calculated network metrics to compare environmental to reference sequences. These metrics reflected the divergence between both types of sequences and provided an effective way to search for evolutionary relevant diversity, further validated by phylogenetic placements. Our results showed that the percentage of unicellular holozoan diversity remains hidden. We found novelties in several lineages, especially in Acanthoecida choanoflagellates. We also identified a potential new holozoan group that could not be assigned to any of the described extant clades. Data on geographical distribution showed that, although ubiquitous, each unicellular holozoan lineage exhibits a different distribution pattern. We also identified a positive association between new animal hosts and the ichthyosporean symbiont Creolimax fragrantissima, as well as for other holozoans previously reported as free-living. Overall, our analyses provide a fresh perspective into the diversity and ecology of unicellular holozoans, highlighting the amount of undescribed diversity.

Diversity and ecology of protists revealed by metabarcoding

“…Remarkably, however, it is worth noting that the catalogue of these major protist groups has not been fundamentally altered since environmental sequencing, even high-throughput metabarcoding, came into play. In fact, less than a handful of highranking environmental lineages branching outside of established major groups have been discovered since the beginning of environmental sequencing (e.g., Picozoa 57 , Rappemonads 58 , or a novel group related to animals called MASHOL 59 ), some of which have now been assimilated to known groups (e.g., Rappemonads belong to haptophytes 60 ).…”

Freshwater protists: unveiling the unexplored in a large floodplain system

“…Matsen et al, 2010;Dunthorn et al, 2014;Mahé et al, 2017;Metz et al, 2019b). Gene similarity network analysis combines the similarity between the query ASVs and with reference sequences (Lynch et al, 2012;Filker et al, 2015;Filker et al, 2016;Arroyo et al, 2020). Arroyo et al (2020) use different network metrics to compare the divergence between both sequences, providing a direct overview of the groups of ASVs that probably represent novel taxonomic groups.…”

“…Matsen et al ., 2010; Dunthorn et al ., 2014; Mahé et al ., 2017; Metz et al ., 2019b). Gene similarity network analysis combines the similarity between the query ASVs and with reference sequences (Lynch et al ., 2012; Filker et al ., 2015; Filker et al ., 2016; Arroyo et al ., 2020). Arroyo et al .…”

Highlight: A Search for New Species on the High Seas

“…This striking gap between what we know and what we do not greatly limits our understanding of the evolution of various taxonomic groups and features. In an article in Genome Biology and Evolution titled “Gene similarity networks unveil a potential novel unicellular group closely related to animals from the Tara Oceans expedition,” researchers at the Institut de Biologia Evolutiva in Spain and the Institut de Systématique, Évolution, Biodiversité in France shed light on the uncharacterized microbial biodiversity of the world’s oceans and reveal how the discovery of new lineages may aid in addressing unanswered evolutionary questions ( Arroyo et al. 2020 ).…”

“…Sequences belonging to the novel Holozoa group MASHOL are shown as red triangles and highlighted in the black circle. Reprinted from Arroyo et al (2020) .…”