Heavy Metal Stress Alters the Response of the Unicellular Cyanobacterium Synechococcus elongatus PCC 7942 to Nitrogen Starvation

Abstract

Non-diazotrophic cyanobacteria are unable to fix atmospheric nitrogen and rely on combined nitrogen for growth and development. In the absence of combined nitrogen sources, most non-diazotrophic cyanobacteria, e.g., Synechocystis sp. PCC 6803 or Synechococcus elongatus PCC 7942, enter a dormant stage called chlorosis. The chlorosis process involves switching off photosynthetic activities and downregulating protein biosynthesis. Addition of a combined nitrogen source induces the regeneration of chlorotic cells in a process called resuscitation. As heavy metals are ubiquitous in the cyanobacterial biosphere, their influence on the vegetative growth of cyanobacterial cells has been extensively studied. However, the effect of heavy metal stress on chlorotic cyanobacterial cells remains elusive. To simulate the natural conditions, we investigated the effects of long-term exposure of S. elongatus PCC 7942 cells to both heavy metal stress and nitrogen starvation. We were able to show that elevated heavy metal concentrations, especially for Ni2+, Cd2+, Cu2+ and Zn2+, are highly toxic to nitrogen starved cells. In particular, cells exposed to elevated concentrations of Cd2+ or Ni2+ were not able to properly enter chlorosis as they failed to degrade phycobiliproteins and chlorophyll a and remained greenish. In resuscitation assays, these cells were unable to recover from the simultaneous nitrogen starvation and Cd2+ or Ni2+ stress. The elevated toxicity of Cd2+ or Ni2+ presumably occurs due to their interference with the onset of chlorosis in nitrogen-starved cells, eventually leading to cell death.

Comparative Genomic Analysis of the DUF34 Protein Family Suggests Role as a Metal Ion Chaperone or Insertase

“…The CutA1 protein family (formerly known as DUF190) has historically been linked to divalent cation tolerance, copper sensitivity, and cytotoxicity (PF03091; IPR004323; COG1324) [ 143 , 144 , 145 , 146 , 147 , 148 , 149 ]; however, due to characteristics of the quaternary structure (trimers form ferredoxin-like folds [ 150 ]), roles in signal transduction and regulation have also been suggested [ 151 , 152 , 153 ]. More recently, refute of the protein’s involvement in metal ion tolerance has led to predictions of CutA1 proteins acting in a small molecule carrier or signaling capacity [ 154 , 155 ]. Still, the functions of all three “CutA” proteins remain under-defined with only small attributions put forward for each, in addition to CutA1: CutA2 (DsbD) is thought to have disulfide oxidoreductase activity [ 156 ]; and CutA3 (YjdC) has been annotated as an HTH-type transcriptional regulator (TetR/AcrR family), more specifically a negative regulator of nitroreductase NfnB [ 157 ].…”

Glucosidase Inhibitors Screening in Microalgae and Cyanobacteria Isolated from the Amazon and Proteomic Analysis of Inhibitor Producing Synechococcus sp. GFB01

“…Although abiotic stress, whether due to salinity [ 85 ], light cycles [ 54 , 86 ], heavy metals [ 87 ] or even nutritional stress [ 88 ], can increase protein expression, by activating alternative pathways in the face of metabolic imbalance [ 69 , 89 , 90 ], in the present work the reduction of nitrate in the culture medium, despite not significantly influencing the growth of the strain or the production of Chlorophyll α ( Table 1 ), and even presenting a higher protein content on day 15—with 693 μg/mL under stress against 546 μg/mL in BG- 11—resulted in the identification of fewer proteins, with only 14 exclusive to this condition ( Figure 4 A). The correlation of higher protein expression with nitrate availability has also been observed in Synechococcus sp.…”

Diurnal metabolic control in cyanobacteria requires perception of second messenger signaling molecule c-di-AMP by the carbon control protein SbtB

“…Nitrogen starvation was induced by shifting the cells to nitrogen-free BG 11 medium (BG 11 0 ) with an initial optical density at 750 nm (OD 750 ) of 0.5 and kept under constant light of 50 to 100 μE. For resuscitation assays, samples were taken after 7 and 14 days of nitrogen starvation, and the resuscitation was induced by shifting the cultures back to BG 11 n , as described previously ( 19 , 46 ). The osmotic stress was generated by addition of 50 to 600 mM sorbitol to BG 11 n , as indicated.…”