The systematics of single-celled cyanobacteria represents a major challenge due to morphological convergence and application of various taxonomic concepts. The genus Cyanothece is one of the most problematic cases, as the name has been applied to oval-shaped coccoid cyanobacteria lacking sheaths with little regard to their phylogenetic position and details of morphology and ultrastructure. Hereby we analyze an extensive set of complementary genetic and phenotypic evidence to disentangle the relationships among these cyanobacteria. We provide diagnostic characters to separate the known genera Cyanothece, Gloeothece, and Aphanothece, and provide a valid description for Crocosphaera gen. nov. We describe two new genera, Rippkaea and Zehria, to characterize two distinct phylogenetic lineages outside the previously known genera. We further describe 13 new species in total including Cyanothece svehlovae, Gloeothece aequatorialis, G. aurea, G. bryophila, G. citriformis, G. reniformis, Gloeothece tonkinensis, G. verrucosa, Crocosphaera watsonii, C. subtropica, C. chwakensis, Rippkaea orientalis, and Zehria floridana to recognize the intrageneric diversity as rendered by polyphasic analysis. We discuss the close relationship of free-living cyanobacteria from the Crocosphaera lineage to nitrogen-fixing endosymbionts of marine algae. The current study includes several experimental strains (Crocosphaera and "Cyanothece") important for the study of diazotrophy and the global oceanic nitrogen cycle, and provides evidence suggesting ancestral N2 -fixing capability in the chroococcalean lineage.

Department of Botany University of South Bohemia Faculty of Science Branišovská 1760 CZ 37005 České Budějovice Czech Republic

Department of Parasitology Faculty of Science University of South Bohemia Branišovská 1760 CZ 37005 České Budějovice

Firenze Unit Institute for Complex Systems National Research Council of Italy via Madonna del Piano 10 1 500 19 Sesto Fiorentino Italy

Firenze Unit Institute of Ecosystem Study National Research Council of Italy via Madonna del Piano 10 1 500 19 Sesto Fiorentino Italy

Institute for the Conservation and Valorization of Cultural Heritage National Research Council of Italy via Madonna del Piano 10 1 500 19 Sesto Fiorentino Italy

Institute of Botany Academy of Sciences of the Czech Republic Dukelská 135 CZ 37982 Třeboň Czech Republic

Institute of Hydrobiology Biology Centre The Czech Academy of Sciences Na Sádkách 7 CZ 37005 České Budějovice Czech Republic

John Carroll University Department of Biology University Heights Ohio 44118 USA

References provided by Crossref.org

The balance between photosynthesis and respiration explains the niche differentiation between Crocosphaera and Cyanothece

Electron & Biomass Dynamics of Cyanothece Under Interacting Nitrogen & Carbon Limitations

Temporal Patterns and Intra- and Inter-Cellular Variability in Carbon and Nitrogen Assimilation by the Unicellular Cyanobacterium Cyanothece sp. ATCC 51142

Quantitative models of nitrogen-fixing organisms

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MH678556, MH678564