Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development

Cyanobacteria were among the oldest organisms to undertake oxygenic photosynthesis and have an essential impact on the atmosphere and carbon/nitrogen cycles on the planet. The thylakoid membrane of cyanobacteria represents an intricate compartment that houses a variety of multi-component (pigment–)p...

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Main Authors: Fang Huang, Arturas Grauslys, Tuomas Huokko, Eva Caamaño Gutiérrez, Andrew R. Jones, Lu-Ning Liu
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/12/23/3967
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author Fang Huang
Arturas Grauslys
Tuomas Huokko
Eva Caamaño Gutiérrez
Andrew R. Jones
Lu-Ning Liu
author_facet Fang Huang
Arturas Grauslys
Tuomas Huokko
Eva Caamaño Gutiérrez
Andrew R. Jones
Lu-Ning Liu
author_sort Fang Huang
collection DOAJ
description Cyanobacteria were among the oldest organisms to undertake oxygenic photosynthesis and have an essential impact on the atmosphere and carbon/nitrogen cycles on the planet. The thylakoid membrane of cyanobacteria represents an intricate compartment that houses a variety of multi-component (pigment–)protein complexes, assembly factors, and regulators, as well as transporters involved in photosynthetic light reactions, and respiratory electron transport. How these protein components are incorporated into membranes during thylakoid formation and how individual complexes are regulated to construct the functional machinery remains elusive. Here, we carried out an in-depth statistical analysis of the thylakoid proteome data obtained during light-induced thylakoid membrane biogenesis in the model cyanobacterium <i>Synechococcus</i> elongatus PCC 7942. A total of 1581 proteins were experimentally quantified, among which 457 proteins demonstrated statistically significant variations in abundance at distinct thylakoid biogenesis stages. Gene Ontology and KEGG enrichment analysis revealed that predominantly photosystems, light-harvesting antennae, ABC transporters, and pathway enzymes involved in oxidative stress responses and protein folding exhibited notable alternations in abundance between high light and growth light. Moreover, through cluster analysis the 1581 proteins were categorized into six distinct clusters that have significantly different trajectories of the change in their abundance during thylakoid development. Our study provides insights into the physiological regulation for the membrane integration of protein components and functionally linked complexes during the cyanobacterial TM biogenesis process. The findings and analytical methodologies developed in this study may be valuable for studying the global responses of TM biogenesis and photosynthetic acclimation in plants and algae.
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spelling doaj.art-72cf4467f84d4a1bb9d571f0ecb414622023-12-08T15:23:48ZengMDPI AGPlants2223-77472023-11-011223396710.3390/plants12233967Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane DevelopmentFang Huang0Arturas Grauslys1Tuomas Huokko2Eva Caamaño Gutiérrez3Andrew R. Jones4Lu-Ning Liu5Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool L69 7BE, UKCyanobacteria were among the oldest organisms to undertake oxygenic photosynthesis and have an essential impact on the atmosphere and carbon/nitrogen cycles on the planet. The thylakoid membrane of cyanobacteria represents an intricate compartment that houses a variety of multi-component (pigment–)protein complexes, assembly factors, and regulators, as well as transporters involved in photosynthetic light reactions, and respiratory electron transport. How these protein components are incorporated into membranes during thylakoid formation and how individual complexes are regulated to construct the functional machinery remains elusive. Here, we carried out an in-depth statistical analysis of the thylakoid proteome data obtained during light-induced thylakoid membrane biogenesis in the model cyanobacterium <i>Synechococcus</i> elongatus PCC 7942. A total of 1581 proteins were experimentally quantified, among which 457 proteins demonstrated statistically significant variations in abundance at distinct thylakoid biogenesis stages. Gene Ontology and KEGG enrichment analysis revealed that predominantly photosystems, light-harvesting antennae, ABC transporters, and pathway enzymes involved in oxidative stress responses and protein folding exhibited notable alternations in abundance between high light and growth light. Moreover, through cluster analysis the 1581 proteins were categorized into six distinct clusters that have significantly different trajectories of the change in their abundance during thylakoid development. Our study provides insights into the physiological regulation for the membrane integration of protein components and functionally linked complexes during the cyanobacterial TM biogenesis process. The findings and analytical methodologies developed in this study may be valuable for studying the global responses of TM biogenesis and photosynthetic acclimation in plants and algae.https://www.mdpi.com/2223-7747/12/23/3967cyanobacteriaphotosynthesisacclimationthylakoid membranemembrane biogenesisproteome
spellingShingle Fang Huang
Arturas Grauslys
Tuomas Huokko
Eva Caamaño Gutiérrez
Andrew R. Jones
Lu-Ning Liu
Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
Plants
cyanobacteria
photosynthesis
acclimation
thylakoid membrane
membrane biogenesis
proteome
title Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
title_full Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
title_fullStr Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
title_full_unstemmed Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
title_short Dynamic Changes in the Thylakoid Proteome of Cyanobacteria during Light-Regulated Thylakoid Membrane Development
title_sort dynamic changes in the thylakoid proteome of cyanobacteria during light regulated thylakoid membrane development
topic cyanobacteria
photosynthesis
acclimation
thylakoid membrane
membrane biogenesis
proteome
url https://www.mdpi.com/2223-7747/12/23/3967
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