Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation

Abstract

Summary Cyanobacteria evolved sophisticated mechanisms allowing them to cope with environmental depletion of combined nitrogen. Here, we describe progress in understanding the processes involved in acclimation of nondiazotrophic cyanobacteria to nitrogen shortage, known as nitrogen chlorosis. The process includes immediate metabolic changes and degradation of light harvesting complexes as well as long‐term acclimation responses. Consequently, quiescent cells substantially differing from vegetative cells are obtained. Thus, the process leading to these considerable metabolic and morphological changes is referred to as a developmental program. Current understanding of the relevant regulatory processes depicts an intricate mechanism involving modulation of transcription activators by proteinaceous interacting components, as well as by small metabolites reporting the energy status and carbon–nitrogen balance of the cell. In addition, we describe in detail the quiescent state characterizing cells under prolonged starvation and the process of recovery from this dormant chlorotic state. Accumulated data provide an in depth understanding of the mechanisms accompanying the cycling of cyanobacterial cells between vegetative growth, the quiescent‐state and the recovery program, allowing them to regain proliferative growth upon nutrient replenishment.

Relationship Between Glycerolipids and Photosynthetic Components During Recovery of Thylakoid Membranes From Nitrogen Starvation-Induced Attenuation in Synechocystis sp. PCC 6803

“…Consistent with our data, Ogawa and Sonoike (2016) determined the "true" maximum quantum yield of PSII (Fv/Fm) in Synechocystis by eliminating the interference from phycocyanin fluorescence and revealed that the Fv/Fm around 0.8, which was similar to the value observed in land plants, substantially decreased with N starvation. Inactivation of PSII may reduce a risk of photodamage from light energy that exceeds the photosynthetic capacity in N-starved cells with decreased cellular metabolism (Forchhammer and Schwarz, 2019).…”

“…Doello et al (2018) revealed that the N-starved chlorotic cells maintain ATP levels to 20-25% of nutrientsufficient cells. As discussed by Forchhammer and Schwarz (2019), the cyclic electron transport around PSI may be retained in N-starved cells to maintain ATP levels and cell viability during chlorosis.…”

“…Proteins are the most abundant component of the thylakoid membrane and account for 50-70% of total thylakoid components by weight (Murata et al, 1981;Chapman et al, 1983;Omata and Murata, 1983). Nitrogen (N) starvation strongly affects protein homeostasis and thus thylakoid functions including the photosynthetic electron transport (Forchhammer and Schwarz, 2019). The most prominent alteration in proteome with N starvation is extensive degradation of PBSs, which are composed of phycobiliproteins with covalently bound phycobilins and non-pigmented linker proteins.…”

“…Proteins in PBSs constitute up to 50% of total protein in the cyanobacterial cell under optimal growth conditions and thus can provide massive nutrients with degradation in response to N starvation (Collier and Grossman, 1992;Görl et al, 1998). Another objective of the active degradation of PBSs may be avoidance of photodamage caused by over reduction of photosynthetic electron carriers due to the low metabolic activity during N starvation (Forchhammer and Schwarz, 2019). The levels of photosystem proteins also decrease under N-starved conditions, with PSII subunits more strongly degraded than PSI subunits (Spät et al, 2018).…”

Uncultured marine cyanophages encode for active NblA, phycobilisome proteolysis adaptor protein

“…First, dismantling of the PBS releases nutrients in the form of amino acids; second, reduced cellular metabolism under starvation might lead to over-excitation and therefore, degradation and uncoupling of the PBS serve as a mechanism to reduce electron transfer rate under such conditions. Multiple studies of PBS degradation have provided insight into the mechanism underlying this process (Forchhammer and Schwarz 2018).…”