Genetic and physiological responses to light quality in a deep ocean ecotype of Ostreococcus, an ecologically important photosynthetic picoeukaryote.

Phytoplankton are exposed to dramatic variations in light quality when cells are carried by upwelling or downwelling currents or encounter sediment. We investigated the potential impact of light quality changes in Ostreococcus, a key marine photosynthetic picoeukaryote, by analysing changes in its transcriptome, pigment content, and photophysiology after acclimation to monochromatic red, green, or blue light. The clade B species RCC809, isolated from the deep euphotic zone of the tropical Atlantic Ocean, responded to blue light by accelerating cell division at the expense of storage reserves and by increasing the relative level of blue-light-absorbing pigments. It responded to red and green light by increasing its potential for photoprotection. In contrast, the clade A species OTTH0595, which originated from a shallow water environment, showed no difference in photosynthetic properties and minor differences in carotenoid contents between light qualities. This was associated with the loss of candidate light-quality responsive promoter motifs identified in RCC809 genes. These results demonstrate that light quality can have a major influence on the physiology of eukaryotic phytoplankton and suggest that different light quality environments can drive selection for diverse patterns of responsiveness and environmental niche partitioning.

Cyanobacteria and Eukaryotic Algae Use Different Chemical Variants of Vitamin B12.

Eukaryotic microalgae and prokaryotic cyanobacteria are the major components of the phytoplankton. Determining factors that govern growth of these primary producers, and how they interact, is therefore essential to understanding aquatic ecosystem productivity. Over half of microalgal species representing marine and freshwater habitats require for growth the corrinoid cofactor B12, which is synthesized de novo only by certain prokaryotes, including the majority of cyanobacteria. There are several chemical variants of B12, which are not necessarily functionally interchangeable. Cobalamin, the form bioavailable to humans, has as its lower axial ligand 5,6-dimethylbenzimidazole (DMB). Here, we show that the abundant marine cyanobacterium Synechococcus synthesizes only pseudocobalamin, in which the lower axial ligand is adenine. Moreover, bioinformatic searches of over 100 sequenced cyanobacterial genomes for B12 biosynthesis genes, including those involved in nucleotide loop assembly, suggest this is the form synthesized by cyanobacteria more broadly. We further demonstrate that pseudocobalamin is several orders of magnitude less bioavailable than cobalamin to several B12-dependent microalgae representing diverse lineages. This indicates that the two major phytoplankton groups use a different B12 currency. However, in an intriguing twist, some microalgal species can use pseudocobalamin if DMB is provided, suggesting that they are able to remodel the cofactor, whereas Synechococcus cannot. This species-specific attribute implicates algal remodelers as novel and keystone players of the B12 cycle, transforming our perception of the dynamics and complexity of the flux of this nutrient in aquatic ecosystems.

Identification of major zinc-binding proteins from a marine cyanobacterium: insight into metal uptake in oligotrophic environments.

Marine cyanobacteria make a significant contribution to primary production whilst occupying some of the most nutrient poor regions of the world's oceans. The low bioavailability of trace metals can limit the growth of phytoplankton in ocean waters, but only scarce data are available on the requirements of marine microbes for zinc. Recent genome mining studies suggest that marine cyanobacteria have both uptake systems for zinc and proteins that utilize zinc as a cofactor. In this study, the oligotrophic strain Synechococcus sp. WH8102 was grown at different zinc concentrations. Using metalloproteomics approaches, we demonstrate that even though this organism's growth was not affected by extremely low zinc levels, cells accumulated significant quantities of zinc, which was shown to be protein-associated by 2D liquid chromatography and ICP-MS. This indicates that the mechanisms for zinc uptake in Synechococcus sp. WH8102 are extremely efficient. Significantly, expression of SYNW2224, a putative porin, was up-regulated during growth in zinc-depleted conditions. Furthermore, along with 30 other proteins, SYNW2224 was captured by immobilised zinc affinity chromatography, indicating the presence of surface-exposed site(s) with metal-binding capacity. It is proposed that this porin plays a role in high-affinity zinc uptake in this and other cyanobacteria.