July 22, 2020
Journal Article

Proteomic insights into phycobilisome degradation, a selective and tightly controlled process in the fast growing cyanobacterium Synechococcus elongatus UTEX 2973

Aparna Nagarajan
Mowei Zhou
Amelia Nguyen
Michelle Liberton
Komal Kedia
Tujin Shi
Anil Shukla
Thomas Fillmore
Carrie Nicora
Jon Jacobs
Himadri Pakrasi

Abstract

Phycobilisomes (PBSs) are large (3-5 megadalton) pigment-protein complexes found in cyanobacteria that associate with thylakoid membranes and harvest light primarily for photosystem II. PBSs consist of highly ordered assemblies of pigmented phycobiliproteins (PBPs) and linker proteins that can account for up to half of the soluble protein in cells. Cyanobacteria adjust to changing environmental conditions by modulating PBS size and number. In response to nutrient depletion such as nitrogen (N) deprivation, PBSs are degraded in an extensive, tightly controlled, and reversible process. In Synechococcus elongatus UTEX 2973, a fast growing cyanobacterium with a doubling time of two hours, the process of PBS degradation is very rapid. We observed that 80% of PBSs per cell were degraded in six hours during N starvation under optimal light and CO2 conditions and this process follows a log linear decay. Photosystems also underwent changes as an immediate consequence of N depletion. Proteomic analysis during the time course of PBS degradation and re-synthesis revealed multiple proteoforms of the PBPs with partially degraded phycocyanobilin (PCB) pigments. Additionally, NblA, a small proteolysis adaptor previously identified as essential in PBS degradation, was characterized and validated with targeted mass spectrometry. NblA levels rise from essentially 0 to 25000 copies per cell within 30 minutes of N depletion. Levels of NblA correlate with the rate of decrease in phycocyanin (PC) during PBS degradation. Implications of this correlation on the overall mechanism of PBS degradation during N deprivation are discussed.

Revised: July 22, 2020 | Published: August 16, 2019

Citation

Nagarajan A., M. Zhou, A.Y. Nguyen, M.L. Liberton, K. Kedia, T. Shi, and P.D. Piehowski, et al. 2019. "Proteomic insights into phycobilisome degradation, a selective and tightly controlled process in the fast growing cyanobacterium Synechococcus elongatus UTEX 2973." Biomolecules 9, no. 8:Article Number 374. PNNL-SA-146394. doi:10.3390/biom9080374