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

PLoS One. 2018 Dec 19;13(12):e0209115. doi: 10.1371/journal.pone.0209115. eCollection 2018.

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.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Biological
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Computational Biology
  • Gene Expression
  • Light
  • Oxygen / metabolism
  • Photosynthesis / physiology*
  • Photosystem II Protein Complex / metabolism*
  • Phylogeny
  • Prochlorococcus / metabolism*
  • Protein Isoforms / metabolism
  • Species Specificity
  • Synechococcus / metabolism*

Substances

  • Bacterial Proteins
  • Photosystem II Protein Complex
  • Protein Isoforms
  • Oxygen

Associated data

  • Dryad/10.5061/dryad.8dc747r

Grants and funding

This work was funded by a Natural Science and Engineering Research Council of Canada Discovery Team Grant to AMC and DAC (grant number: 435405-2013), from the Canada Research Chair Program (DC), using equipment funded by the Canadian Foundation for Innovation and the New Brunswick Innovation Foundation (DC). DAC was supported by the Microbiology Institute of the Czech Academy of Science through project CZ.02.2.69/0.0/0.0/16_027/0007990 of the European Union Researcher Mobility program. EMB, BET, CDM and JRM received Independent Student Research Grants from Mount Allison University. The funders had no role in study design, data collection or analysis, decision to publish, or preparation of the manuscript.