To multicellularity and back again: Description of two new coccoid genera (Portococcus gen. nov. and Pseudanabaenococcus gen. nov.) in the basal “filamentous” order Pseudanabaenales, Cyanobacteria

Despite recent efforts in taxonomic revision of phylogenetically basal photosynthetic cyanobacteria, cryptic diversity and recurrence of simple plesiomorphic morphotypes has continued to appear in phylogenies with poorly characterized “Synechococcus” and “Pseudanabaena” strains. Herein, one of the prominent undefined unicellular lineages was resolved as a monophyletic group of taxa that have lost multicellularity within the otherwise filamentous order Pseudanabaenales. Genome sequencing coupled with the classical polyphasic taxonomic analysis based on the 16S rRNA gene and the ITS rRNA region sequence comparisons, light and transmission electron microscopy, and source habitat record have congruently supported the description of two novel genera, Portococcus, with four new species, and Pseudanabaenococcus, with a single new species. The whole-genome phylogeny was essential for the accurate assessment of phylogenetic relationships between the genera and families and is hereby highly recommended as a new standard integrated in the polyphasic taxonomy of cyanobacteria. Records of the new taxa from a variety of freshwater habitats and one terrestrial cave habitat in geographically distant regions have indicated the need for further investigation to discover the full extent of cryptic diversity in these deep-branching clades. The loss of filamentous forms within the first group in cyanobacterial evolution that had invented it offers an excellent model for future study of the genetic and physiological mechanisms of early prokaryotic multicellularity.