Nitrogen or Sulfur Starvation Differentially Affects Phycobilisome Degradation and Expression of the nblA Gene in Synechocystis Strain PCC 6803

Abstract

Nitrogen (N) limitation in cyanobacteria is well documented: a reduced growth rate is observed, accompanied by a cessation of phycobiliprotein synthesis and an ordered degradation of phycobilisomes (PBS). This leads to a dramatic bleaching phenomenon known as chlorosis. In Synechococcus strain PCC 7942, bleaching due to PBS degradation is also observed under sulfur (S) or phosphorus (P) limitation, and all three are under the control of the nblA gene product, a 59-amino-acid polypeptide which is overexpressed under N, S, and P starvation (J. L. Collier, and A. R. Grossman, EMBO J. 13:1039-1047, 1994). Cyanobase sequence data for Synechocystis strain PCC 6803 indicate the presence of two tandem open reading frames (sll0452 and sll0453) homologous to nblA. We cloned the two genes, identified a unique 5 mRNA end suggestive of a single transcription start site, and studied nblA expression under conditions of N or S starvation by Northern hybridization: transcripts were detected only under N starvation (no signal is detected in replete medium or with S starvation), whether nblA1 or nblA2 was used as a probe. Mutations in nblA1 and nblA2 were constructed by insertion of a kanamycin cassette; both mutations were nonbleaching under N starvation. Synechocystis strain PCC 6803 does not bleach under S starvation, consistent with the absence of nblA induction in these conditions. These results were confirmed by analysis of the PBS components: sequential degradation of phycocyanin and associated linkers was observed only under conditions of N starvation. This indicates differences between Synechocystis strain PCC 6803 and Synechococcus strain PCC 7942 in their regulatory and signaling pathways leading to N-and S-starved phenotypes.

Immunolocalization of NblA, a protein involved in phycobilisome turnover, during heterocyst differentiation in cyanobacteria

“…The stimuli that lead to phycobilisome degradation may vary depending on the organism (Richaud et al, 2001). At present NblA proteins have been studied almost exclusively in unicellular non-N 2 -fixing cyanobacteria, for which phycobilisome degradation appears to be a very important adaptative mechanism that improves survival of the cyanobacteria under high light conditions and during nutrient limitation (Görl et al, 1998;Schwarz & Grossman, 1998;Sauer et al, 2001;van Waasbergen et al, 2002).…”

“…strain PCC 7942 and Synechocystis sp. strain PCC 6803, high levels of nblA transcripts (Grossman et al, 2001;Luque et al, 2001;Richaud et al, 2001), as well as proteins (Baier et al, 2001) accumulate under macronutrient limitation. For filamentous diazotrophic cyanobacteria belonging to sections IV and V (Rippka & Herdman, 1992), the lack of a combined nitrogen source leads to differentiation of heterocysts (cells specialized for aerobic N 2 fixation).…”

Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses

“…The pioneering work using this approach led to identification of nblA, a small gene encoding a 59 amino acid polypeptide, which is induced upon starvation (Collier & Grossman, 1994). Subsequently, genes encoding NblA-like peptides were identified and characterized in various cyanobacterial species (Baier et al, 2001;de Alda et al, 2004;Delumeau et al, 2002;Luque et al, 2003;Richaud et al, 2001;Li & Sherman, 2002). In fact, examination of the available complete genomic sequences indicated the existence of at least one nblA homologue in all organisms that possess a phycobilisome (cyanobacteria and red algae).…”

“…Furthermore, different cyanobacterial strains may respond quite differently to various starvation conditions. For example, sulfur starvation causes rapid chlorosis in Synechococcus (Collier & Grossman, 1992), while Synechocystis does not degrade its phycobilisome in response to sulfur deprivation (Richaud et al, 2001).…”

A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation

“…To determine the origin of FNR S in Synechocystis, we tested the effect of nitrogen starvation (known to induce PBS degradation) on the FNR in cell extracts from WT and two mutants in which PBS were not degraded under nitrogen starvation conditions: N1 lacking nblA1, a gene that is induced and necessary for PBS trimming under nitrogen starvation (23), and M55 deficient in ndhB, encoding a subunit of the NDH-I complex (24). The latter mutant exhibits attenuated PBS degradation when nitrogenstarved, probably because of deficient respiration (J.-C.T.…”