Genomic capacities for Reactive Oxygen Species metabolism across marine phytoplankton.

Marine phytoplankton produce and scavenge Reactive Oxygen Species, to support cellular processes, while limiting damaging reactions. Some prokaryotic picophytoplankton have, however, lost all genes encoding scavenging of hydrogen peroxide. Such losses of metabolic function can only apply to Reactive Oxygen Species which potentially traverse the cell membrane outwards, before provoking damaging intracellular reactions. We hypothesized that cell radius influences which elements of Reactive Oxygen Species metabolism are partially or fully dispensable from a cell. We therefore investigated genomes and transcriptomes from diverse marine eukaryotic phytoplankton, ranging from 0.4 to 44 µm radius, to analyze the genomic allocations encoding enzymes metabolizing Reactive Oxygen Species. Superoxide has high reactivity, short lifetimes and limited membrane permeability. Genes encoding superoxide scavenging are ubiquitous across phytoplankton, but the fractional gene allocation decreased with increasing cell radius, consistent with a nearly fixed set of core genes for scavenging superoxide pools. Hydrogen peroxide has lower reactivity, longer intracellular and extracellular lifetimes and readily crosses cell membranes. Genomic allocations to both hydrogen peroxide production and scavenging decrease with increasing cell radius. Nitric Oxide has low reactivity, long intracellular and extracellular lifetimes and readily crosses cell membranes. Neither Nitric Oxide production nor scavenging genomic allocations changed with increasing cell radius. Many taxa, however, lack the genomic capacity for nitric oxide production or scavenging. The probability of presence of capacity to produce nitric oxide decreases with increasing cell size, and is influenced by flagella and colony formation. In contrast, the probability of presence of capacity to scavenge nitric oxide increases with increasing cell size, and is again influenced by flagella and colony formation.

Strain specific differences in rates of Photosystem II repair in picocyanobacteria correlate to differences in FtsH protein levels and isoform expression patterns.

Picocyanobacteria are the numerically dominant photoautotrophs of the oligotrophic regions of Earth's oceans. These organisms are characterized by their small size and highly reduced genomes. Strains partition to different light intensity and nutrient level niches, with differing photosynthetic apparatus stoichiometry, light harvesting machinery and susceptibility to photoinactivation. In this study, we grew three strains of picocyanobacteria: the low light, high nutrient strain Prochlorococcus marinus MIT 9313; the high light, low nutrient Prochlorococcus marinus MED 4; and the high light, high nutrient marine Synechococcus strain WH 8102; under low and high growth light levels. We then performed matched photophysiology, protein and transcript analyses. The strains differ significantly in their rates of Photosystem II repair under high light and in their capacity to remove the PsbA protein as the first step in the Photosystem II repair process. Notably, all strains remove the PsbD subunit at the same rate that they remove PsbA. When grown under low light, MIT 9313 loses active Photosystem II quickly when shifted to high light, but has no measurable capacity to remove PsbA. MED 4 and WH 8102 show less rapid loss of Photosystem II and considerable capacity to remove PsbA. MIT 9313 has less of the FtsH protease thought to be responsible for the removal of PsbA in other cyanobacteria. Furthermore, by transcript analysis the predominant FtsH isoform expressed in MIT 9313 is homologous to the FtsH 4 isoform characterized in the model strain Synechocystis PCC 6803, rather than the FtsH 2 and 3 isoforms thought to be responsible for PsbA degradation. MED 4 on the other hand shows high light inducible expression of the isoforms homologous to FtsH 2 and 3, consistent with its faster rate of PsbA removal. MIT 9313 has adapted to its low light environment by diverting resources away from Photosystem II content and repair.