Photosynthetic Function of Phycobilisomes

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1		Xiang Li	--	1344	2023-06-13 11:11:57	\|
2	format correct	Catherine Yang	Meta information modification	1344	2023-06-14 03:02:03	\|

This entry is adapted from the peer-reviewed paper 10.3390/ijms24119733

The phycobilisome (PBS) is the major light-harvesting apparatus in cyanobacteria and red algae. It is a large multi-subunit protein complex of several megadaltons that is found on the stromal side of thylakoid membranes in orderly arrays. Chromophore lyases catalyse the thioether bond between apoproteins and phycobilins of PBSs.

phycobilisome phycobilin phycobiliprotein assembly

1. Introduction

The phycobilisome (PBS) was first identified by Gantt and Conti ^[1]. PBSs are large chromophore-protein complexes located on the stromal side of thylakoid membranes. As a light-harvesting antenna system, PBSs absorb light between 450 and 650 nm and transmit it efficiently to the reaction centres of the photosynthetic systems of cyanobacteria and red algae.

The main bricks in the spatial arrangement of phycobilisomes are phycobiliproteins (PBPs), which have covalently attached linear open-chain tetrapyrroles called phycobilins, and linker proteins. With the linker proteins, PBPs form the structural backbone of the phycobilisome. Diversity in the number and spatial structure of lyase-catalysed phycobilin binding varies the spectral properties of PBPs. Therefore, phycobilin synthesis, lyase catalysis, and self-assembly of apoproteins and the auxiliary linker proteins are essential for the assembly of phycobiliproteins and the structural and functional stability of the PBS.

2. Light Energy Capture and Transfer in PBS

As a light-harvesting complex, phycobilisomes absorb light energy through pigment molecules and transmit it to the reaction centres of PSII ^[2]. The structure of an intact PBS in complex with PSII from Anabaena sp. strain PCC 7120 was unambiguously resolved using single-particle electron microscopy ^[3]. Moreover, research focusing on the in situ structures of PBS-PSII-PSI-LHC megacomplexes from the red alga Porphyridium purpureum provided interaction details between PBS, PSII, and PSI at near-atomic resolution using cryogenic electron tomography. All these works contribute a solid structural basis for unravelling the mechanisms of the PBS-PSII-PSI-LHC megacomplex assembly, the efficient energy transfer from PBS to the two photosystems, and the regulation of energy distribution between PSII and PSI ^[4].

Aquatic environments present a unique light environment, and different species of small cyanobacteria and red algae can survive through absorbing a wide range of wavelengths. Phycobilisomes exhibit various and flexible absorption peaks to ensure the efficiency of capturing and transmitting light energy in deep water; in particular, the blue–green light that can penetrate deep water. In addition, PBSs form huge arrays on the thylakoid membranes as antennae. The arrangement of phycobilisomes on the thylakoid membranes is light-intensity-dependent, and their arrangements may be both disordered and ordered. At a light intensity of 15 W·m⁻² (medium light), the PBSs on the thylakoid membrane are clustered in discrete regions, while at a light intensity of 6 W·m⁻² (low light), uniformly sized PBSs on the thylakoid membrane are orderly arranged in parallel ^[5].

Interestingly, cyanobacteria exhibit a form of photomorphogenesis termed chromatic acclimation (CA), and one of the characteristics of CA is the regulation of the pigment composition of PBPs to optimise light absorption for photosynthesis, thus adapting to the light environment in water ^[6]. The proximity of chromophores in adjacent PBSs suggests that there might also be light energy transfer between PBSs ^[7].

In the PBS structure, the energy is first received by the PE or PEC at the distal part of the rod and transmitted to the APC core through the PC. Finally, it is transferred to PSII or PSI through the multidomain core–membrane linker (LCM) at the end of the core complex. There are two possible energy transfer pathways in this process: direct energy transfers from PBS to PSI (PBS→PSI transfer) and indirect transfer through PSII (PBS→PSII→PSI transfer) ^[8]. In terms of the energy level of light absorption, these four PBPs can be further divided into three types: high energy (PE and PEC), medium energy (PC), and low energy (APC). According to the arrangement of PBPs in the PBS, the PBPs form an overall organisation from high to low energy in PBS. Through this holistic organisation, the absorbed excitation energy can be transferred to the auxiliary chlorophyll of the photosystem quickly, efficiently, and directionally. In addition, APC contributes to the excitation of energy from peripheral rods of the PBS or from directly absorbed red light to auxiliary chlorophyll in the photosystem ^[9].

These large protein complexes capture incident sunlight and transfer the energy to PSII or partially to PSI. This process is achieved through forming PBS-PSII-PSI complexes. Linker proteins play a key role in the formation of modified complexes. ApcE and ApcF are responsible for forming protrusions at the base of the PBS core that fit with the pores on one side of the PSII cell membrane, allowing the PBS and PSII to be tightly connected, which is necessary for the transmission of light energy from PBS to PSII ^[3]. The abundant aromatic amino acid benzene rings on the linker proteins can also form π–π interactions with the tetrapyrrole rings of surrounding pigment molecules, which are involved in regulating the energy state of the pigment molecules to ensure efficient unidirectional energy transfer ^[10].

3. Light Acclimation of PBS

The structure and specialised function of the PBS allows captured light energy to be transferred to the photosynthetic reaction centres with more than 95% efficiency ^[11]. However, excessive light harvesting can also cause damage to cyanobacteria, so cyanobacteria have evolved a photoprotection mechanism called non-photochemical quenching (NPQ) that rapidly converts excess excited energy into heat before it causes damage. However, this process leads to a reduction in the efficiency of light energy conversion. A photoprotection mode is mediated by orange carotenoid protein (OCP), which is the only known carotenoid-activated photoreceptor, and only exists in cyanobacteria to play a role in controlling the photosynthetic mechanism of light capture. It is known to change from OCP^O to OCP^R after absorbing redundant blue–green light, and then four OCP^R form two dimers which are bound to PBS, respectively, leading to NPQ. Notably, not every PBS is equally sensitive to NPQ, and only one of the three PBS conformational states reported associations with the OCP^R ^[12]. The difference in the conformational state is generated through switching the position of the two rods, which regulates light harvesting.

To adapt to changes in environmental conditions, the composition and function of PBSs would change accordingly. Light intensity has the greatest influence on the composition of the rod and the ratio of PC:APC so as to yield a maximum production of PC under optimal photon flux. Other environmental factors also change the composition of the rods. For example, light colour and temperature can change the PC:PE ratio ^[13]. The photosynthetic electron transfer rate of PSII also affects the structure of the PBS. The ratio of PBS to chlorophyll protein content is influenced by the electron transfer rate when the required phytochrome is sufficient. Changes in copper ion concentration affect the stability of PBS, and changes in the structural stability of PBS follow the same trend as changes in the rate of electron transfer associated with copper ion concentration, and the structural stability of PBS decreases with the decrease in electron transfer rate, which may be related to structural changes in the rods. Iron deficiency inhibits PBS synthesis but does not affect the stability of PBS.

Degradation of PBS plays an important role in photoprotection, cell maintenance, growth, and development in a constantly changing environment. During nitrogen limitation, PBSs in cells are degraded to avoid excessive light uptake and to allocate effective nitrogen to functions essential for growth and survival ^[14]. As a large nutrient reserve, the degradation of PBSs can provide essential amino acids for metabolic processes, and low levels of photosynthesis and loss of pigments are essential for cell survival during nitrogen, sulphur, or phosphorus depletion. NblB and NblA are essential components for phycocyanin degradation under starvation conditions, during which NblB levels decrease approximately twofold and directly mediate pigment degradation through chromophore segregation. In contrast, NblA is highly expressed during starvation and may bind to one or two PBS complexes, destabilising the PBS complex and initiating proteochrome degradation ^[15]. NblB-dependent PC degradation did not occur in the absence of NblA, so NblB has a dependent effect on NblA ^[16]. Recent studies have found that NblD plays a critical role in the coordinated catabolism of PBSs and, thus, is a factor in the genetically programmed response to nitrogen starvation ^[17].

References

Gantt, E.; Conti, S.F. Phycobiliprotein localization in algae. Brookhaven Symp. Biol. 1966, 19, 393–405.
Sui, S.F. Structure of Phycobilisomes. Annu. Rev. Biophys. 2021, 50, 53–72.
Chang, L.; Liu, X.; Li, Y.; Liu, C.C.; Yang, F.; Zhao, J.; Sui, S.F. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 2015, 25, 726–737.
You, X.; Zhang, X.; Cheng, J.; Xiao, Y.; Ma, J.; Sun, S.; Zhang, X.; Wang, H.W.; Sui, S.F. In situ structure of the red algal phycobilisome-PSII-PSI-LHC megacomplex. Nature 2023, 616, 199–206.
Folea, I.M.; Zhang, P.; Aro, E.M.; Boekema, E.J. Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett. 2008, 582, 1749–1754.
Montgomery, B.L. Seeing new light: Recent insights into the occurrence and regulation of chromatic acclimation in cyanobacteria. Curr. Opin. Plant. Biol. 2017, 37, 18–23.
Zheng, L.; Zheng, Z.; Li, X.; Wang, G.; Zhang, K.; Wei, P.; Zhao, J.; Gao, N. Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes. Nat. Commun. 2021, 12, 5497.
Ueno, Y.; Aikawa, S.; Niwa, K.; Abe, T.; Murakami, A.; Kondo, A.; Akimoto, S. Variety in excitation energy transfer processes from phycobilisomes to photosystems I and II. Photosynth. Res. 2017, 133, 235–243.
Soulier, N.; Bryant, D.A. The structural basis of far-red light absorbance by allophycocyanins. Photosynth. Res. 2021, 147, 11–26.
Ma, J.; You, X.; Sun, S.; Wang, X.; Qin, S.; Sui, S.F. Structural basis of energy transfer in Porphyridium purpureum phycobilisome. Nature 2020, 579, 146–151.
Zhang, Z.; Lambrev, P.H.; Wells, K.L.; Garab, G.; Tan, H.S. Direct observation of multistep energy transfer in LHCII with fifth-order 3D electronic spectroscopy. Nat. Commun. 2015, 6, 7914.
Domínguez-Martín, M.A.; Sauer, P.V.; Kirst, H.; Sutter, M.; Bína, D.; Greber, B.J.; Nogales, E.; Polívka, T.; Kerfeld, C.A. Structures of a phycobilisome in light-harvesting and photoprotected states. Nature 2022, 609, 835–845.
Chenu, A.; Keren, N.; Paltiel, Y.; Nevo, R.; Reich, Z.; Cao, J. Light Adaptation in Phycobilisome Antennas: Influence on the Rod Length and Structural Arrangement. J. Phys. Chem. B 2017, 121, 9196–9202.
Yoshihara, A.; Kobayashi, K. Photosynthesis and Cell Growth Trigger Degradation of Phycobilisomes during Nitrogen Limitation. Plant Cell Physiol. 2022, 62, 189–199.
Nagarajan, A.; Zhou, M.; Nguyen, A.Y.; Liberton, M.; Kedia, K.; Shi, T.; Piehowski, P.; Shukla, A.; Fillmore, T.L.; Nicora, C.; et al. Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973. Biomolecules 2019, 9, 374.
Levi, M.; Sendersky, E.; Schwarz, R. Decomposition of cyanobacterial light harvesting complexes: NblA-dependent role of the bilin lyase homolog NblB. Plant J. 2018, 94, 813–821.
Krauspe, V.; Fahrner, M.; Spät, P.; Steglich, C.; Frankenberg-Dinkel, N.; Maček, B.; Schilling, O.; Hess, W.R. Discovery of a small protein factor involved in the coordinated degradation of phycobilisomes in cyanobacteria. Proc. Natl. Acad. Sci. USA 2021, 118, e2012277118.

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Xiang Li

Wenwen Hou

Jiaxi Lei

Hui Chen

Qiang Wang

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Update Date: 14 Jun 2023

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1. Introduction

2. Light Energy Capture and Transfer in PBS

3. Light Acclimation of PBS

References