The Braarudosphaera bigelowii genome reveals cellular remodeling around a nitrogen-fixing organelle

Abstract

Braarudosphaera bigelowii hosts the nitrogen-fixing cyanobacterial organelle UCYN-A, or the nitroplast, but the absence of a reference genome has limited investigation of the genomic features accompanying this association. Here, we present nuclear and organellar genome resources for the cultured B. bigelowii strain FR-21. The assembly comprises a 472.1-Mb nuclear genome together with representative nitroplast, chloroplast, and mitochondrial genomes of 1.49 Mb, 107 kb, and 44 kb, respectively. The four genomic compartments have strongly differentiated GC compositions, consistent with their distinct evolutionary origins. The large nuclear genome does not appear to reflect a corresponding expansion of protein-coding capacity. Repeat annotation indicates that approximately 77% of the nuclear assembly is repetitive, leaving approximately 108 Mb of nonrepetitive sequence containing roughly 16,000 predicted protein-coding genes. Phylogenomic analysis places B. bigelowii within the expected diversity of haptophytes, indicating that its unusual diazotrophic lifestyle is not associated with an anomalous phylogenetic position. Comparative analysis of nitrogen metabolism genes reveals extensive remodeling of host nitrogen acquisition and assimilation. B. bigelowii lacks major components required for nitrate and nitrite assimilation and has reduced capacity to use urea, cyanate, and several internally recycled nitrogen sources. In contrast, ammonium transport and the glutamine synthetase-glutamate synthase pathway are retained. This combination suggests reduced flexibility in nitrogen use and a host metabolism increasingly centered on ammonium supplied by the nitroplast. B. bigelowii also encodes an expanded set of flavodoxin and cryptochrome genes. Eleven of 14 flavodoxin candidates and 21 of 39 cryptochrome candidates contained motifs linked to nitroplast targeting. Together with previous evidence that some of these proteins are abundantly imported into the nitroplast, these expansions point to host-encoded roles in nitroplast redox metabolism and diel regulation. These genome resources establish a foundation for investigating nitroplast protein import, host-organelle metabolic integration, and the genomic consequences of acquiring an intracellular nitrogen-fixing compartment. They further show that the evolution of the B. bigelowii-UCYN-A relationship involved substantial remodeling of genome architecture and nitrogen metabolism in both partners.