Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses

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 expre...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Rajib Saha, Deng Liu, Allison Hoynes-O’Connor, Michelle Liberton, Jingjie Yu, Maitrayee Bhattacharyya-Pakrasi, Andrea Balassy, Fuzhong Zhang, Tae Seok Moon, Costas D. Maranas, Himadri B. Pakrasi
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2016
Materias:
Acceso en línea:https://doaj.org/article/84a5ca6c94bd4fad88bd6f7cb6d9d780
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:84a5ca6c94bd4fad88bd6f7cb6d9d780
record_format dspace
spelling oai:doaj.org-article:84a5ca6c94bd4fad88bd6f7cb6d9d7802021-11-15T15:50:16ZDiurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses10.1128/mBio.00464-162150-7511https://doaj.org/article/84a5ca6c94bd4fad88bd6f7cb6d9d7802016-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00464-16https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Cyanobacteria are photosynthetic microbes that use energy from sunlight and CO2 as feedstock. Certain cyanobacterial strains are amenable to facile genetic manipulation, thus enabling synthetic biology and metabolic engineering applications. Such strains are being developed as a chassis for the sustainable production of food, feed, and fuel. To this end, a holistic knowledge of cyanobacterial physiology and its correlation with gene expression patterns under the diurnal cycle is warranted. In this report, a genomewide transcriptional analysis of Synechocystis PCC 6803, the most widely studied model cyanobacterium, sheds light on the global coordination of cellular processes during diurnal periods. Furthermore, we found that, in addition to light, the redox level of NADP(H) is an important endogenous regulator of diurnal entrainment of Synechocystis PCC 6803.Rajib SahaDeng LiuAllison Hoynes-O’ConnorMichelle LibertonJingjie YuMaitrayee Bhattacharyya-PakrasiAndrea BalassyFuzhong ZhangTae Seok MoonCostas D. MaranasHimadri B. PakrasiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 3 (2016)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Rajib Saha
Deng Liu
Allison Hoynes-O’Connor
Michelle Liberton
Jingjie Yu
Maitrayee Bhattacharyya-Pakrasi
Andrea Balassy
Fuzhong Zhang
Tae Seok Moon
Costas D. Maranas
Himadri B. Pakrasi
Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
description 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. IMPORTANCE Cyanobacteria are photosynthetic microbes that use energy from sunlight and CO2 as feedstock. Certain cyanobacterial strains are amenable to facile genetic manipulation, thus enabling synthetic biology and metabolic engineering applications. Such strains are being developed as a chassis for the sustainable production of food, feed, and fuel. To this end, a holistic knowledge of cyanobacterial physiology and its correlation with gene expression patterns under the diurnal cycle is warranted. In this report, a genomewide transcriptional analysis of Synechocystis PCC 6803, the most widely studied model cyanobacterium, sheds light on the global coordination of cellular processes during diurnal periods. Furthermore, we found that, in addition to light, the redox level of NADP(H) is an important endogenous regulator of diurnal entrainment of Synechocystis PCC 6803.
format article
author Rajib Saha
Deng Liu
Allison Hoynes-O’Connor
Michelle Liberton
Jingjie Yu
Maitrayee Bhattacharyya-Pakrasi
Andrea Balassy
Fuzhong Zhang
Tae Seok Moon
Costas D. Maranas
Himadri B. Pakrasi
author_facet Rajib Saha
Deng Liu
Allison Hoynes-O’Connor
Michelle Liberton
Jingjie Yu
Maitrayee Bhattacharyya-Pakrasi
Andrea Balassy
Fuzhong Zhang
Tae Seok Moon
Costas D. Maranas
Himadri B. Pakrasi
author_sort Rajib Saha
title Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
title_short Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
title_full Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
title_fullStr Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
title_full_unstemmed Diurnal Regulation of Cellular Processes in the Cyanobacterium <italic toggle="yes">Synechocystis</italic> sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses
title_sort diurnal regulation of cellular processes in the cyanobacterium <italic toggle="yes">synechocystis</italic> sp. strain pcc 6803: insights from transcriptomic, fluxomic, and physiological analyses
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/84a5ca6c94bd4fad88bd6f7cb6d9d780
work_keys_str_mv AT rajibsaha diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT dengliu diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT allisonhoynesoconnor diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT michelleliberton diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT jingjieyu diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT maitrayeebhattacharyyapakrasi diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT andreabalassy diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT fuzhongzhang diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT taeseokmoon diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT costasdmaranas diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
AT himadribpakrasi diurnalregulationofcellularprocessesinthecyanobacteriumitalictoggleyessynechocystisitalicspstrainpcc6803insightsfromtranscriptomicfluxomicandphysiologicalanalyses
_version_ 1718427468956696576