Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host

A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N -fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, , has penetrated the cell envelope of the host, , and lives inside the host cytoplasm. How the partners interact, including how the symbiont sustains high rates of N fixation, is unstudied. Since has evaded isolation, heterologous expression of genes in model laboratory organisms was performed to identify the function of proteins from the endosymbiont. Gene complementation of a cyanobacterial invertase mutant and expression of the protein in showed that HH01 possesses a neutral invertase that splits sucrose producing glucose and fructose. Several solute-binding proteins (SBPs) of ABC transporters encoded in the genome of HH01 were expressed in , and their substrates were characterized. The selected SBPs directly linked the host as the source of several substrates, e.g. sugars (sucrose and galactose), amino acids (glutamate and phenylalanine), and a polyamine (spermidine), to support the cyanobacterial symbiont. Finally, transcripts of genes encoding the invertase and SBPs were consistently detected in wild populations of collected from multiple stations and depths in the western tropical North Atlantic. Our results support the idea that the diatom host provides the endosymbiotic cyanobacterium with organic carbon to fuel N fixation. This knowledge is key to understanding the physiology of the globally significant symbiosis.