Horizontal gene transfer and reciprocal chimerism in Compactonostoc (Nostocales, Cyanobacteriophyta) with evidence for two new species in the genus

The genus Nostoc has long been known to be polyphyletic, and recent taxonomic work has segregated several Nostoc-like lineages into new genera, including Compactonostoc. Until now, C. shennongjiaensis was the only described species in the genus. In a survey of biological soil crusts from Santa Catalina Island (California, United States), we isolated two Nostoc-like strains that phylogenetically affiliate with Compactonostoc. A polyphasic approach based on morphology, 16S rRNA gene phylogeny, 16S-23S ITS rRNA secondary structures, and cloned ribosomal operons revealed that each strain harbored two highly divergent ribosomal operon types. One operon (Type 2) is closely related to C. shennongjiaensis and contains the two tRNA genes in the ITS rRNA region, whereas the second (Type 1) lacks tRNA genes and is strongly allied to the horizontally acquired Type 1 operon previously reported in Kalymmatonema (as Scytonema hyalinum), indicating an ancient horizontal gene transfer event from an unsampled Nostocaceaen lineage. In one of the isolated strains, we additionally detected two reciprocal chimeric operons (Type 2/1 and Type 1/2), with crossovers in a conserved region of the 16S rRNA gene, demonstrating ongoing recombination between operon types. The ITS rRNA region percent dissimilarity, ITS rRNA region domain structures, and 16S rRNA gene percent similarity, together with consistent morphological differences, support recognition of the two strains as new species of Compactonostoc, C. mediiheterocytium and C. chimera, both clearly distinct from C. shennongjiaensis. Our results document rare ribosomal-operon horizontal gene transfer and reciprocal chimerism in Compactonostoc and highlight the need to examine multiple clones and operons when describing cyanobacterial taxa based on rRNA genes.