Brown algae produce hydrocarbons via fatty acid photodecarboxylase-dependent and -independent pathways

Abstract

Across the tree of life, diverse organisms synthesize hydrocarbons (HCs) from fatty acids using various enzymes. In plants and insects, HCs are typically excreted (e.g. waxes, pheromones), whereas in algae, they seem to be mostly intracellular and membrane-associated. To date, all studied organisms have been found to possess only one HC-forming pathway. In most green algae, unesterified fatty acids are converted into HCs by the algal-specific photoenzyme fatty acid photodecarboxylase (FAP). Other green algae lacking the FAP are able to synthesize HCs via the ECERIFERUM 1/3 (CER1/3) protein. Here, using heterologous expression in E. coli, we show that six FAP homologs belonging to diverse groups of brown algae (Phaeophyceae) are functional. We also demonstrate that Ectocarpus species 7 and Saccharina latissima produce two intracellular HCs during vegetative growth: n-pentadecane (15:0 HC) and n-heneicosahexaene (21:6 HC), which is distinct from the n-heneicosahexaene isomer found in some green algae. Through genome editing, we show that 15:0 HC, likely localized in chloroplast membranes, is synthesized via a FAP-dependent pathway in Ectocarpus, while the 21:6 HC is produced through an unidentified alternative pathway. Our results support the hypothesis that FAP plays a conserved biological role in brown algae. Furthermore, this work provides the first example of a group of organisms harboring a second, distinct HC-forming pathway, which may fulfil a unique biological function.