Diurnal Regulation of Cellular Processes in the Cyanobacterium Synechocystis sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses

Authors

Rajib Saha, Washington UniversityFollow
Deng Liu, Washington University
Allison Hoynes-O’Connor, Washington University
Michelle Liberton, Washington University
Jingjie Yu, Washington University
Maitrayee Bhattacharyya-Pakrasi, Washington University
Andrea Balassy, Washington University
Fuzhong Zhang, Washington University
Tae Seok Moon, Washington University
Costas D. Maranas, The Pennsylvania State University
Himadri B. Pakrasi, Washington University

Date of this Version

2016

Document Type

Article

Citation

Saha R, Liu D, Hoynes-O’Connor A, Liberton M, Yu J, Bhattacharyya-Pakrasi M, Balassy A, Zhang F, Moon TS, Maranas CD, Pakrasi HB. 2016. Diurnal regulation of cellular processes in the cyanobacterium Synechocystis sp. strain PCC 6803: insights from transcriptomic, fluxomic, and physiological analyses. mBio 7(3):e00464-16.

Comments

© 2016 Saha et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Abstract

Synechocystis sp. strain PCC 6803 is the most widely studied model cyanobacterium, with a well-developed omics level knowledgebase. Like the lifestyles of other cyanobacteria, that of Synechocystis PCC 6803 is tuned to diurnal changes in light intensity. In this study, we analyzed the expression patterns of all of the genes of this cyanobacterium over two consecutive diurnal periods. Using stringent criteria, we determined that the transcript levels of nearly 40% of the genes in Synechocystis PCC 6803 show robust diurnal oscillating behavior, with a majority of the transcripts being upregulated during the early light period. Such transcripts corresponded to a wide array of cellular processes, such as light harvesting, photosynthetic light and dark reactions, and central carbon metabolism. In contrast, transcripts of membrane transporters for transition metals involved in the photosynthetic electron transport chain (e.g., iron, manganese, and copper) were significantly upregulated during the late dark period. Thus, the pattern of global gene expression led to the development of two distinct transcriptional networks of coregulated oscillatory genes. These networks help describe how Synechocystis PCC 6803 regulates its metabolism toward the end of the dark period in anticipation of efficient photosynthesis during the early light period. Furthermore, in silico flux prediction of important cellular processes and experimental measurements of cellular ATP, NADP(H), and glycogen levels showed how this diurnal behavior influences its metabolic characteristics. In particular, NADPH/NADP⁺ showed a strong correlation with the majority of the genes whose expression peaks in the light. We conclude that this ratio is a key endogenous determinant of the diurnal behavior of this cyanobacterium.