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Biochimica Et Biophysica Acta.... Apr 2020Cyanobacteria and red-algae share a common light-harvesting complex which is different than all other complexes that serve as photosynthetic antennas - the Phycobilisome... (Review)
Review
Cyanobacteria and red-algae share a common light-harvesting complex which is different than all other complexes that serve as photosynthetic antennas - the Phycobilisome (PBS). The PBS is found attached to the stromal side of thylakoid membranes, filling up most of the gap between individual thylakoids. The PBS self assembles from similar homologous protein units that are soluble and contain conserved cysteine residues that covalently bind the light absorbing chromophores, linear tetra-pyrroles. Using similar construction principles, the PBS can be as large as 16.8 MDa (68×45×39nm), as small as 1.2 MDa (24 × 11.5 × 11.5 nm), and in some unique cases smaller still. The PBS can absorb light between 450 nm to 650 nm and in some cases beyond 700 nm, depending on the species, its composition and assembly. In this review, we will present new observations and structures that expand our understanding of the distinctive properties that make the PBS an amazing light harvesting system. At the end we will suggest why the PBS, for all of its excellent properties, was discarded by photosynthetic organisms that arose later in evolution such as green algae and higher plants.
Topics: Bacterial Proteins; Energy Transfer; Light-Harvesting Protein Complexes; Models, Molecular; Photochemical Processes; Phycobilisomes
PubMed: 31306623
DOI: 10.1016/j.bbabio.2019.07.002 -
Biomolecules Nov 2019The phycobilisome (PBS) is the major light-harvesting complex of photosynthesis in cyanobacteria, red algae, and glaucophyte algae. In spite of the fact that it is very... (Review)
Review
The phycobilisome (PBS) is the major light-harvesting complex of photosynthesis in cyanobacteria, red algae, and glaucophyte algae. In spite of the fact that it is very well structured to absorb light and transfer it efficiently to photosynthetic reaction centers, it has been completely lost in the green algae and plants. It is difficult to see how selection alone could account for such a major loss. An alternative scenario takes into account the role of chance, enabled by (contingent on) the evolution of an alternative antenna system early in the diversification of the three lineages from the first photosynthetic eukaryote.
Topics: Bacterial Proteins; Chlorophyta; Cyanobacteria; Evolution, Molecular; Photosynthesis; Phycobilisomes; Plant Proteins; Rhodophyta
PubMed: 31752285
DOI: 10.3390/biom9110748 -
Photosynthesis Research Oct 2013The phycobilisome (PBS) is an extra-membrane supramolecular complex composed of many chromophore (bilin)-binding proteins (phycobiliproteins) and linker proteins, which... (Review)
Review
The phycobilisome (PBS) is an extra-membrane supramolecular complex composed of many chromophore (bilin)-binding proteins (phycobiliproteins) and linker proteins, which generally are colorless. PBS collects light energy of a wide range of wavelengths, funnels it to the central core, and then transfers it to photosystems. Although phycobiliproteins are evolutionarily related to each other, the binding of different bilin pigments ensures the ability to collect energy over a wide range of wavelengths. Spatial arrangement and functional tuning of the different phycobiliproteins, which are mediated primarily by linker proteins, yield PBS that is efficient and versatile light-harvesting systems. In this review, we discuss the functional and spatial tuning of phycobiliproteins with a focus on linker proteins.
Topics: Light-Harvesting Protein Complexes; Models, Molecular; Phycobiliproteins; Phycobilisomes
PubMed: 24081814
DOI: 10.1007/s11120-013-9905-3 -
International Journal of Molecular... Jun 2023The 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... (Review)
Review
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. Depending on the species, composition, spatial assembly, and, especially, the functional tuning of different phycobiliproteins mediated by linker proteins, PBSs can absorb light between 450 and 650 nm, making them efficient and versatile light-harvesting systems. However, basic research and technological innovations are needed, not only to understand their role in photosynthesis but also to realise the potential applications of PBSs. Crucial components including phycobiliproteins, phycobilins, and lyases together make the PBS an efficient light-harvesting system, and these provide a scheme to explore the heterologous synthesis of PBS. Focusing on these topics, this review describes the essential components needed for PBS assembly, the functional basis of PBS photosynthesis, and the applications of phycobiliproteins. Moreover, key technical challenges for heterologous biosynthesis of phycobiliproteins in chassis cells are discussed.
Topics: Phycobilisomes; Phycobilins; Phycobiliproteins; Photosynthesis; Rhodophyta
PubMed: 37298688
DOI: 10.3390/ijms24119733 -
Annales de Microbiologie 1983This report describes the properties of a relatively simple phycobilisome, Synechococcus 6301 (Anacystis nidulans). Morphology. -- Examination of wild type and mutant... (Review)
Review
This report describes the properties of a relatively simple phycobilisome, Synechococcus 6301 (Anacystis nidulans). Morphology. -- Examination of wild type and mutant phycobilisomes by electron microscopy has shown them to have two morphologically differing substructures when seen in "face-view". There is a core consisting of two contiguous objects, disc-like in face-view projection, 115 A in diameter, and six rods, each composed of several stacked discs 60 A thick and 120 A in diameter, which radiate from the core in a hemidiscoidal arrangement. Each of the core components consists of four discs approximately 30 A thick. Rod substructures. -- Each of the discs in the rod substructure is a phycocyanin hexamer held together by interaction with a specific linker polypeptide, i. e., it has the composition (alpha beta)6 . X, where X is the linker polypeptide and alpha beta a phycocyanin monomer. The disc proximal to the core is an (alpha beta)6 . 27,000 complex. A small portion, Mr approximately 2,000,, of the Mr 27,000 polypeptide is essential to the attachment of this disc to the core. From studies of phycobilisomes from nitrogen-starved cells, and from mutants containing lowered amounts of phycocyanin relative to allophycocyanin, the second disc has been established to be an (alpha beta)6 . 33,000 complex. Either (alpha beta)6 . 33,000 or (alpha beta)6 . 30,000 complexes occupy the positions in the rods distal to the (alpha beta)6 .33,000 discs. Core substructure. -- Structural studies on the core and on core-rod junctions were greatly facilitated by the isolation of a mutant, strain AN112, which produces phycobilisomes with rods only one disc in length but with normal cores. Partial dissociation of these incomplete phycobilisomes under a variety of conditions, and separation and characterization of the resulting sub-complexes, has led to the determination of the composition of four distinct "trimeric" complexes, each of which is present in two copies per phycobilisome. These complexes, which account for the composition of the core, are as follows: (alpha beta)3AP . 10,500 with lambda maxF at 662 nm; (alpha beta)3AP with lambda maxF at 660 nm; (alpha 2AP alpha APB beta 3AP) . 10,500 with lambda maxF at 680 nm; where apha AP and alpha AFB are alpha subunits of allophycocyanin and allophycocyanin B, respectively, and beta AP is a subunit common to these two biliproteins; (alpha beta)2 AP . 18,300 . 40,000* . 11,000* with lambda maxF at 680 nm, where the Mr 40,000* and 11,000* polypeptides are derived from a Mr 75,000 polypeptide by tryptic digestion.(ABSTRACT TRUNCATED AT 400 WORDS)
Topics: Cyanobacteria; Light-Harvesting Protein Complexes; Macromolecular Substances; Microscopy, Electron; Models, Biological; Nitrogen; Phycobilisomes; Phycocyanin; Pigments, Biological; Plant Proteins; Spectrum Analysis; Structure-Activity Relationship
PubMed: 6416125
DOI: 10.1016/s0769-2609(83)80103-3 -
Nature Apr 2023In oxygenic photosynthetic organisms, light energy is captured by antenna systems and transferred to photosystem II (PSII) and photosystem I (PSI) to drive...
In oxygenic photosynthetic organisms, light energy is captured by antenna systems and transferred to photosystem II (PSII) and photosystem I (PSI) to drive photosynthesis. The antenna systems of red algae consist of soluble phycobilisomes (PBSs) and transmembrane light-harvesting complexes (LHCs). Excitation energy transfer pathways from PBS to photosystems remain unclear owing to the lack of structural information. Here we present in situ structures of PBS-PSII-PSI-LHC megacomplexes from the red alga Porphyridium purpureum at near-atomic resolution using cryogenic electron tomography and in situ single-particle analysis, providing interaction details between PBS, PSII and PSI. The structures reveal several unidentified and incomplete proteins and their roles in the assembly of the megacomplex, as well as a huge and sophisticated pigment network. This work provides a solid structural basis for unravelling the mechanisms of PBS-PSII-PSI-LHC megacomplex assembly, efficient energy transfer from PBS to the two photosystems, and regulation of energy distribution between PSII and PSI.
Topics: Energy Transfer; Light-Harvesting Protein Complexes; Photosynthesis; Photosystem I Protein Complex; Photosystem II Protein Complex; Phycobilisomes; Porphyridium; Cryoelectron Microscopy; Single Molecule Imaging
PubMed: 36922595
DOI: 10.1038/s41586-023-05831-0 -
Biochemistry Apr 2023Phycobilisomes (PBSs) are the major photosynthetic light-harvesting complexes in cyanobacteria and red algae. PBS, a multisubunit protein complex, has two major...
Phycobilisomes (PBSs) are the major photosynthetic light-harvesting complexes in cyanobacteria and red algae. PBS, a multisubunit protein complex, has two major interfaces that comprise intrinsically disordered regions (IDRs): rod-core and core-membrane. IDRs do not form regular, three-dimensional structures on their own. Their presence in the photosynthetic pigment-protein complexes portends their structural and functional importance. A recent model suggests that PB-loop, an IDR located on the PBS subunit ApcE and C-terminal extension (CTE) of the PBS subunit ApcG, forms a structural protrusion on the PBS core-membrane side, facing the thylakoid membrane. Here, the structural synergy between the rod-core region and the core-membrane region was investigated using quantitative mass spectrometry (MS). The AlphaFold-predicted CpcG-CTE structure was first modeled onto the PBS rod-core region, guided and justified by the isotopically encoded structural MS data. Quantitative cross-linking MS analysis revealed that the structural proximity of the PB-loop in ApcE and ApcG-CTE is significantly disturbed in the absence of six PBS rods, which are attached to PBS via CpcG-CTE, indicative of drastic conformational changes and decreased structural integrity. These results suggest that CpcG-rod attachment on the PBS rod-core side is essentially required for the PBS core-membrane structural assembly. The hypothesized long-range synergy between the rod-core interface (where the orange carotenoid protein also functions) and the terminal energy emitter of PBS must have important regulatory roles in PBS core assembly, light-harvesting, and excitation energy transmission. These data also lend strategies that genetic truncation of the light-harvesting antennas aimed for improved photosynthetic productivity must rely on an in-depth understanding of their global structural integrity.
Topics: Phycobilisomes; Cyanobacteria; Thylakoids; Mass Spectrometry
PubMed: 36943676
DOI: 10.1021/acs.biochem.3c00047 -
Nature Communications Dec 2023Phycobilisomes (PBS) are antenna megacomplexes that transfer energy to photosystems II and I in thylakoids. PBS likely evolved from a basic, inefficient form into the...
Phycobilisomes (PBS) are antenna megacomplexes that transfer energy to photosystems II and I in thylakoids. PBS likely evolved from a basic, inefficient form into the predominant hemidiscoidal shape with radiating peripheral rods. However, it has been challenging to test this hypothesis because ancestral species are generally inaccessible. Here we use spectroscopy and cryo-electron microscopy to reveal a structure of a "paddle-shaped" PBS from a thylakoid-free cyanobacterium that likely retains ancestral traits. This PBS lacks rods and specialized ApcD and ApcF subunits, indicating relict characteristics. Other features include linkers connecting two chains of five phycocyanin hexamers (CpcN) and two core subdomains (ApcH), resulting in a paddle-shaped configuration. Energy transfer calculations demonstrate that chains are less efficient than rods. These features may nevertheless have increased light absorption by elongating PBS before multilayered thylakoids with hemidiscoidal PBS evolved. Our results provide insights into the evolution and diversification of light-harvesting strategies before the origin of thylakoids.
Topics: Thylakoids; Phycobilisomes; Cryoelectron Microscopy; Photosystem I Protein Complex; Bacterial Proteins; Cyanobacteria
PubMed: 38049400
DOI: 10.1038/s41467-023-43646-9 -
Nature Sep 2022Phycobilisome (PBS) structures are elaborate antennae in cyanobacteria and red algae. These large protein complexes capture incident sunlight and transfer the energy...
Phycobilisome (PBS) structures are elaborate antennae in cyanobacteria and red algae. These large protein complexes capture incident sunlight and transfer the energy through a network of embedded pigment molecules called bilins to the photosynthetic reaction centres. However, light harvesting must also be balanced against the risks of photodamage. A known mode of photoprotection is mediated by orange carotenoid protein (OCP), which binds to PBS when light intensities are high to mediate photoprotective, non-photochemical quenching. Here we use cryogenic electron microscopy to solve four structures of the 6.2 MDa PBS, with and without OCP bound, from the model cyanobacterium Synechocystis sp. PCC 6803. The structures contain a previously undescribed linker protein that binds to the membrane-facing side of PBS. For the unquenched PBS, the structures also reveal three different conformational states of the antenna, two previously unknown. The conformational states result from positional switching of two of the rods and may constitute a new mode of regulation of light harvesting. Only one of the three PBS conformations can bind to OCP, which suggests that not every PBS is equally susceptible to non-photochemical quenching. In the OCP-PBS complex, quenching is achieved through the binding of four 34 kDa OCPs organized as two dimers. The complex reveals the structure of the active form of OCP, in which an approximately 60 Å displacement of its regulatory carboxy terminal domain occurs. Finally, by combining our structure with spectroscopic properties, we elucidate energy transfer pathways within PBS in both the quenched and light-harvesting states. Collectively, our results provide detailed insights into the biophysical underpinnings of the control of cyanobacterial light harvesting. The data also have implications for bioengineering PBS regulation in natural and artificial light-harvesting systems.
Topics: Bacterial Proteins; Energy Transfer; Photosynthesis; Phycobilisomes; Sunlight; Synechocystis
PubMed: 36045294
DOI: 10.1038/s41586-022-05156-4 -
Journal of the American Chemical Society May 2023The phycobilisome is the primary light-harvesting antenna in cyanobacterial and red algal oxygenic photosynthesis. It maintains near-unity efficiency of energy transfer...
The phycobilisome is the primary light-harvesting antenna in cyanobacterial and red algal oxygenic photosynthesis. It maintains near-unity efficiency of energy transfer to reaction centers despite relying on slow exciton hopping along a relatively sparse network of highly fluorescent phycobilin chromophores. How the complex maintains this high efficiency remains unexplained. Using a two-dimensional electronic spectroscopy polarization scheme that enhances energy transfer features, we directly watch energy flow in the phycobilisome complex of sp. PCC 6803 from the outer phycocyanin rods to the allophycocyanin core. The observed downhill flow of energy, previously hidden within congested spectra, is faster than timescales predicted by Förster hopping along single rod chromophores. We attribute the fast, 8 ps energy transfer to interactions between rod-core linker proteins and terminal rod chromophores, which facilitate unidirectionally downhill energy flow to the core. This mechanism drives the high energy transfer efficiency in the phycobilisome and suggests that linker protein-chromophore interactions have likely evolved to shape its energetic landscape.
Topics: Phycobilisomes; Photosynthesis; Energy Transfer; Synechocystis
PubMed: 37200045
DOI: 10.1021/jacs.3c01799