Abstract
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.
Highlights
Picocyanobacteria, comprised of marine Synechococcus and Prochlorococcus, are the numerically dominant group of phytoplankton performing oxygenic photosynthesis in the oligotrophic regions of Earth’s oceans [1], together contributing between 32 and 80% of oceanic primary productivity [2,3,4,5,6]
It is clear that these strains, which are adapted to different ecological niches, have very different strategies to cope with damage of their PSII reaction centres caused by high light
The measurable rates of PSII repair and PsbA removal and the higher FtsH hexamer to PsbA ratio for MIT 9313 grown at 90 μmol photons m-2 s-1 suggests that when the cells have been transitioned gradually to the higher light level over a period of generations, they are capable of FtsH 2/3 synthesis even though they lack the ability to induce that capacity over a short period of 90 minutes as measured here
Summary
Picocyanobacteria, comprised of marine Synechococcus and Prochlorococcus, are the numerically dominant group of phytoplankton performing oxygenic photosynthesis in the oligotrophic regions of Earth’s oceans [1], together contributing between 32 and 80% of oceanic primary productivity [2,3,4,5,6]. Zorz et al [22] examined the photophysiology and photosynthetic protein stoichiometry in three strains of picocyanobacteria: the high light, high nutrient Synechococcus WH 8102; the high light, low nutrient Prochlorococcus MED 4; and the low light, high nutrient Prochlorococcus MIT 9313 They showed that when grown under similar conditions of light and temperature, MIT 9313 has a much higher ratio of PSI:PSII than do MED 4 or WH 8102. Partensky et al [23] have recently shown that oxygen evolution rates differ between Prochlorococcus and Synechococcus strains, with PCC 9511 (equivalent to MED 4) achieving the highest oxygen evolution per PSII, an effect that increased with irradiance, while the low light strains MIT 9313 and SS120 show lower oxygen evolution per PSII that decreased with increased irradiance These results show that different ecotypes of picocyanobacteria differ significantly in the photosynthetic strategies that they employ to survive in their respective niches
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