Comparative Genomics Insights Into the Evolutionary Disparities Between Nitroplast-Evolved Ecotype UCYN-A2 and Its...

UCYN-A is a phenomenal diazotrophic cyanobacterium with significant ecological importance. UCYN-A1 and UCYN-A2 are the two most abundant ecotypes. Recently, the striking discovery of nitroplast, a novel N₂-fixing organelle in cultured B. bigelowii/UCYN-A2 endosymbiont, indicated the possibility that UCYN-A2 has evolved beyond endosymbiosis to an early phase of organellogenesis. This study addresses the following critical question: What evolutionary heterogeneity has emerged between UCYN-A1 and UCYN-A2? To investigate this issue, we comprehensively compared a total of seven genomes from UCYN-A2 and UCYN-A1. Under similar genome organizations, GC content, and gene composition, we still detected abundant genetic differences, including group-unique orthogroups, ANI below 85%, and 577 UCYN-A2-unique INDELs in single-copy orthologous genes (SCOGs). Moreover, we also focused on the orthologous genes of 40 metabolic-pathway genes in nitroplast. In addition to high-informative SNPs and INDELs possessing distinct interlineage differences, we traced abundant codon usage "signatures" that serve as lineage-unique molecular markers. Most notably, we successfully established a strain-level identification map for UCYN-A strains using codon aversion motifs, which represents the first case study of this approach in bacteria. In summary, all the comparative results reported here collectively indicate that UCYN-A1 and UCYN-A2 have evolved remarkable genomic heterogeneities. Furthermore, the findings of this work will definitely promote our current understanding of codon aversion and the evolution of UCYN-A.