Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973.

Aparna Nagarajan,Michelle Liberton,Komal Kedia,Carrie Nicora,Thomas L Fillmore,Richard D Smith,Paul Piehowski,Mowei Zhou,Himadri B Pakrasi,Tujin Shi,Amelia Y Nguyen,Anil Shukla,Jon M Jacobs,David W Koppenaal

doi:10.3390/biom9080374

Abstract

Phycobilisomes (PBSs) are large (3–5 megadalton) pigment-protein complexes 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, with 80% of PBSs per cell degraded in six hours under optimal light and CO2 conditions. Proteomic analysis during PBS degradation and re-synthesis revealed multiple proteoforms of PBPs with partially degraded phycocyanobilin (PCB) pigments. NblA, a small proteolysis adaptor essential for PBS degradation, was characterized and validated with targeted mass spectrometry. NblA levels rose from essentially 0 to 25,000 copies per cell within 30 min of N depletion, and correlated with the rate of decrease in phycocyanin (PC). Implications of this correlation on the overall mechanism of PBS degradation during N deprivation are discussed.

Highlights

IntroductionThe protein complexes of the photosynthetic electron transport chain are located in the internal thylakoid membrane system
Cyanobacteria are photosynthetic microbes that can convert sunlight into chemical energy usingCO2 as a carbon source
The PBS light harvesting antenna complex can account for 50% or more of soluble cellular protein

Summary

Introduction

The protein complexes of the photosynthetic electron transport chain are located in the internal thylakoid membrane system. Large extrinsic phycobilisome (PBS) antenna complexes associate with the cytoplasmic side of the thylakoid membranes and harvest light energy for the photosynthetic apparatus [1,2]. Biomolecules 2019, 9, 374 cyanobacteria based on their potential to produce biofuels and biochemicals in a carbon-neutral manner. Most cyanobacteria to date have shown slow rates of growth and biomass accumulation compared to heterotrophic organisms such as yeast, precluding their use in industrial settings. The faster growth rate in UTEX 2973 is attributed to adjustments in the photosystem and light harvesting components [4]. Given that many details of PBS modulation and regulation are not well-characterized in cyanobacteria, it is important to understand how cyanobacteria respond to changing environmental conditions in order to optimize the use of these organisms as bioproduction platforms

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