You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic. For video creation, please contact our Academic Video Service.
Version Summary Created by Modification Content Size Created at Operation
1
Victor . V. Kusnetsov
 -- 3082 2023-02-13 11:55:56 |
2 update references and layout
Rita Xu
 Meta information modification 3082 2023-02-14 02:23:58 |

Video Upload Options

We provide professional Academic Video Service to translate complex research into visually appealing presentations. Would you like to try it?
No, upload directly Yes

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Stadnichuk, I.N.; Kusnetsov, V.V. Phycobilisomes and Phycobiliproteins. Encyclopedia. Available online: https://encyclopedia.pub/entry/41157 (accessed on 16 July 2025).
Stadnichuk IN, Kusnetsov VV. Phycobilisomes and Phycobiliproteins. Encyclopedia. Available at: https://encyclopedia.pub/entry/41157. Accessed July 16, 2025.
Stadnichuk, Igor N., Victor V. Kusnetsov. "Phycobilisomes and Phycobiliproteins" Encyclopedia, https://encyclopedia.pub/entry/41157 (accessed July 16, 2025).
Stadnichuk, I.N., & Kusnetsov, V.V. (2023, February 13). Phycobilisomes and Phycobiliproteins. In Encyclopedia. https://encyclopedia.pub/entry/41157
Stadnichuk, Igor N. and Victor V. Kusnetsov. "Phycobilisomes and Phycobiliproteins." Encyclopedia. Web. 13 February, 2023.
Phycobilisomes and Phycobiliproteins
Edit
This entry is adapted from the peer-reviewed paper 10.3390/ijms24032290

Eukaryotic photosynthesis arose in the course of evolution as a result of the incorporation of an unstored cyanobacterium and its transformation into chloroplasts by an ancestral heterotrophic eukaryotic cell. The pigment apparatus of earlier evolved  Archaeplastida algae and other later algal phyla turned out to be arranged in the same way having pigment-protein complexes of photosystem I (PS I), photosystem II (PS II) and antenna complex. PS I and PS II are characterized by uniform structures, while the light-harvesting antennae have undergone a number  of changes.

chlorophyll cyanobacteria endosymbiosis oxygenic photosynthetics phycobiliproteins Phycobilisomes

1. Introduction

Cyanobacteria developed oxygenic photosynthesis 2.6–2.5 billion years ago (BYA) [1]. Approximately 1.9 BYA, after endosymbiotic uptake by a hetetrotrophic eukaryotic host cell of a cyanobacterium, possibly related to the present primitive genus Gloeomargarita and its evolution into a plastid, the first autotrophic eukaryote arose [2][3][4][5]. This one, common photosynthetic ancestor without a definite name (one possible name—Protoarchaeplastida), which has not survived to our time after primary endosymbiosis, underwent divergence into three eukaryotic lines [6][7]. According to the phylogenomic data, first, 1.7–1.6 BYA, Glaucophyta (blue branch) was separated from the common evolutionary tree [8]; later, 100–200 MYA (million years ago), red algae, or Rhodophyta, (red branch) emerged from the remaining common evolutionary stem of red and green algae; and finally, 1.1 BYA green algae appeared [9]. These three groups of photosynthetics, having the common name Archaeplastida and also called Plantae (Figure 1A) have double membrane plastids and coexist in the biosphere, together with cyanobacteria, up to the present time. In the subsequent events of secondary endosymbioses, green and red microalgae gave rise to photosynthetics with four-membrane plastids (reduced to three membranes in some algae), resulting in various new algal phyla [10]. Together with the three Archaeplastida groups, there are approximately ten major algal taxa. Higher plants inherited the Archaeplastida chloroplasts from the green algae [9].
Ijms 24 02290 g001
Figure 1. Scheme of primary endosymbioses in the origin of plastids. (A) The monophyletic origin of three phyla of Archaeplastida (Glaucophyta, Viridiplantae green algae, and Rhodophyta). The length of the segments connecting the groups in sequence (from left to right) corresponds to the timing of their appearance. The Rhodophyta branch consists of the early isolated subphyla of microalgae Cyanidiophytina and subphyla Rhodophytina [7] containing some micro- and all macrophyte algae. (B) A later independent endosymbiosis that led to the appearance of photosynthetic amoebae.
The monophyletic origin of eukaryotic photosynthetics has one exception. The plastids of a small group of amoebae that exploite photosynthesis originated later than Archaeplastida from an ancestral cyanobacterium of the genus Synechococcus (Figure 1B). Apart from this fact, in the cells of some dinophytic algae, their own secondary plastids were subsequently lost and replaced by the plastids of the engulfed cryptophytic or ciliate algae. This effect has been called tertiary endosymbiosis [6][9][10]. During the repeated emergence of new groups of algae, the two photosystems, PS I and PS II, as the basis of oxygenic photosynthesis, started from cyanobacteria and remained unchanged, but the light harvesting cyanobacterial antenna represented by phycobilisomes (PBSs) underwent changes up to replacement by other antennas, Chl a/b or Chl a/c containing pigment–protein complexes [11][12]. Phycobilisomes and phycobiliproteins in the role of antennas are diverse. The greatest contribution to the understanding of their structure and function has come from the study of the pigment apparatus of cyanobacteria.

2. Phycobiliproteins and Phycobilisomes of Cyanobacteria

There are approximately 1500 known species of unicellular, filamentous, and colonial cyanobacteria which are the only prokaryotes that perform oxygenic photosynthesis. Brilliantly colored phycobiliproteins serve as antennas in the pigment apparatus of cyanobacteria, supplying absorbed light energy to PS I and PS II. These chromophorylated water-soluble proteins consist of 16–18 kDa α and 17–20 kDa β polypeptides in a 1-to-1 ratio. Such (αβ)1-heteromonomers spontaneously aggregate into (αβ)3-trimers and then into (αβ)6-hexamers [13]. Four different open-chain phycobilin chromophores, namely, phycocyano-, phycoerythro-, phycourobilin, and cryptoviolin (phycoviolobilin), covalently bind in different ratios via a thioether bond to the Cys residues in both polypeptide subunits. Each α-subunit attaches one or two chromophore groups; each β-polypeptide binds one to four tetrapyrrole chromophores, depending on the specific phycobiliprotein. Each phycobiliprotein has chromophores of one (PC, APC, C-PE) or two different varieties (R-PC, PEC, CU-PEs, and R-PE). A unique trichromatic-variety phycocyanin, R-PC V, was revealed in oceanic Synechococcus sp. WH8102 [14]. As a result, approximately 15 different phycobiliproteins have been described (Table 1).
Table 1. Phycobiliproteins in various photosynthetic clades (except Cryptophyta).
Phycobiliprotein Presence in Photosynthetics
Allophycocyanin (PC, or APC) Cyanobacteria, red, glaucophytic algae, and photosynthetic amoebae
C-phycocyanin (PC, or C-PC) Cyanobacteria, glaucophytic algae, photosynthetic amoebae, and some red algae
Phycoerythrocyanin (PEC) Some cyanobacteria
R-phycocyanin (R-PC, or R-PC I) Red algae
R-PC II, R-PC III, R-PC IV and R-PC V Cyanobacteria
C-phycoerythrin (C-PE) Cyanobacteria
CU-phycoerythrin (CU-PE) Cyanobateria
B- and b-phycoerythrins (B-PE and b-PE) Red algae
R-phycoerythrin (R-PE) Red algae
Colorless linker proteins of about 30 kDa bind disc-shaped hexamers and trimers into cylindrical rods, and these, in turn, assemble into PBSs consisting of two main parts: the APC core and several peripheral rods of other phycobiliproteins surrounding the central core. PBSs of the vast majority of cyanobacteria are hemidiscoidal. Three main morphological types of cyanobacterial PBSs have been observed: (1) with a two-cylindrical core and six fan-shaped lateral cylinders; (2) with a three-cylindrical core and six cylinders; (3) with a five-cylindrical core (three major plus two semicylinders) and eight lateral cylinders (Figure 2A–C).
Ijms 24 02290 g002
Figure 2. Morphological types of cyanobacterial PBSs. (A) Hemidiscoidal PBS with the bicylindrical core. (B) The most typical hemidiscoidal PBS with the tricylindrical core and six lateral cylinders. (C) PBS with the pentacylindrical core and eight lateral cylinders. (D) Bundle-shaped PBS (Gloeobacter type). APC —light blue; PC —blue; PE —red color.
Bundle-shaped PBSs of the genus Gloeobacter have a somewhat unusual architecture with only vertical lateral cylinders (Figure 2D). This morphology saves space on the membrane surface, since cyanobacteria of this genus have no thylakoids and all PBSs are located on the cytoplasmic membrane [15]. When, for some reason, altered conventional PBSs in mutant cyanobacterial cells cannot properly attach to the thylakoid membrane, the energy feeding of PS I is provided by newly synthesized small cylindrical PBSs anchored to PS I by the special CpcG2 polypeptide linker [16][17]. Some cyanobacteria, such as Calothrix sp., can vary their PC and/or PE ratio in PBS depending on the light quality. This phenomenon, realized in several variants, is known as complementary chromatic adaptation (CCA) [18].
In the PBS, absorbed solar energy is funneled from the lateral cylinders to the core and eventually to the terminal longwavelength emitters - chromophorylated ApcD and ApcF varieties of APC subunits and the ApcE (Lcm) - chromophorylated large core-membrane linker protein located in the bottom APC cylinders. From collectively acted terminal emitters, the energy rapidly rolls to PS I and PS II [19][20][21]. Regarding PS II, there has long been a general consensus that in the plane of the thylakoid membrane, PBSs are disposed on the outer surface of PS II dimers [22].
The situation with PS I is more complicated [23][24][25][26]. In cyanobacteria, PS I mainly forms trimers with a certain share of monomers [27][28]. In contrast to the PS II dimers [22], the surface of PS I shows a major protrusion of three hydrophilic polypeptide subunits (PsaC, PsaD, and PsaE), which extends into the cytoplasm [27][28] and prevents a tight binding of PBS to PS I trimer due to its threefold symmetry. Computer modeling demonstrated the docking of PBS to the PS I monomer only, corresponding to a realization of a highly likely energy transfer between these two pigment–protein complexes [29].
Along with the “common” PBSs and the “common” cyanobacteria, there are other species that have caught everyone’s attention.

2.1. Prochlorophyta: Chlorophyll b-Containing Cyanobacteria

Prochlorophyta, or Prochlorales, is a mixed group of cyanobacteria containing Chl a/b-proteins instead of PBS as a photosynthetic antenna. Few known Prochlorophyta members form three genera, namely, Prochlorococcus, Prochloron, and Prochlorothrix, with cells having green or greenish color. The genus Prochlorothrix is represented by two filamentous freshwater species, P. hollandica [30] and P. scandica [31]. P. didemni, the only one known species of the Prochloron genus, is an obligate symbiont of the didemnid ascidia Lissoclinum patella [32]. Various described ecotypes of the genus Prochlorococcus marinus inhabit different geographical areas of the ocean and belong to the most abundant representatives of oceanic photosynthetic picoplankton.
Light-harvesting membrane Chl a/b-binding proteins in Prochlorophyta are derived from the CP43 polypeptide of PS II and are named prochlorophyte Chl-binding (Pcb) proteins [33]  or, less frequently, designated CBP [34], while the Chl a/b-containing antenna in the pigment apparatus of Viridiplantae consists of LHC-polypeptides. According to this type of antenna, Prochlorophyta have stacked regions of thylakoids (Figure 3), making them different from other cyanobacteria [35]. Pcb-proteins form in thylakoid membrane supercomplexes with both photosystems. The PS I trimers are surrounded by a single ring of Pcbs, while dimers of PS II are in contact with two or three divided by a gap Pcb arches [36]. Interestingly, cells of Prochlorococcus contain their divinyl derivatives with the same absorption properties instead of Chls a and b [37]. In addition to the presence of Chls a and b, very small amounts of Chl c variety in Pcb of P. didemnii also cannot be excluded [38].
Ijms 24 02290 g003
Figure 3. Three types of Archaeplastida double membrane chloroplasts. In glaucophytic algae (as well as in photosynthetic amoebae), the chloroplast retains PBSs and the peptidoglycan layer (PG). Red algae retain PBSs, but the peptidoglycan layer is eliminated. In plastids of Viridiplantae, PBSs and peptidoglycan layer are lost while thylakoids form grana regions (similarly to Prochlorophyta).
Of all Prochlorophyta, Prochlorococcus attracts the most attention because of its prominent role in marine primary productivity and the presence of PE [39][40], in addition to its Pcb-antenna proteins. Cyanophages infecting Prochlorococcus contain genes for phycobilin-synthesizing enzymes, and these are expressed in Prochlorococcus, raising further questions of how the PE genes could have been acquired by this species [41]. Various described marine strains of Prochlorococcus belong to one of two ecotypes that are specifically adapted to either low-light or high-light conditions [42][43]. Low-light-adapted ecotypes carry a gene cluster with the cpeA and cpeB genes of PE to produce a small amount of a functional light-absorption pigment. Differences in the sequences of the α and β polypeptide chains and the revealed presence of only one phycourobilin-like attachment site on the α subunit distinguish this red pigment from the known PEs of PBS-containing cyanobacteria. However, the supramolecular organization and aggregation state of PE molecules due to their very low content in thylakoids remain unknown. According to electron micrographs of immunogold-labeled cells, PE is attached to the thylakoid membrane at its lumen side [44].
In the genome of the high-light-adapted strains, only a single and free-standing cpeB gene occurs. This gene encodes a derived form of β-PE, the function of which has remained enigmatic thus far [45]. Interestingly, degenerated forms of the α and β subunits of other cyanobacterial PEs without perturbing their folding, structural stability, and fluorescence functionality were demonstrated to be stable in vitro [46]. Correspondingly, phycobilins are known to serve as single chromophores in cyanobacteriochromes [47]. Therefore, such a degenerated form of PE could change its purpose to being a photoreceptor pigment in Prochlorococcus.

2.2. Chlorophyll d-Containing Cyanobacteria, Acaryochloris marina

Acaryochloris marina is a widespread free-living cyanobacterium that exploits special marine habitats depleted in visible solar radiation and characterized accordingly by an increased proportion of infrared penetrated light. These shady sieve site conditions fully correspond to the microlayer of seawater beneath the body surface of didemnid ascidians, where this species was first described in 1996 [48]. Since then, numerous free-living Acaryochloris strains have been reported to be distributed in various environments, including marine stromatolites, saline lake epilithic biofilms, and some special freshwaters [49].
The pigment apparatus of A. marina is characterized by the presence of Chl d, with absorption shifted to the long-wavelength spectral region compared to Chl a. Different kinds of Chls can readily be distinguished by their S0 → S1 long-wavelength absorption peak positions. This feature helps gain insight into the evolved mechanism for the realization of infrared region photosynthesis. The polypeptide compositions and aggregation states of both the PS I and PS II core complexes (dimers of PS II and monomers/trimers of PS I) of A. marina are similar to those of well studied Chl a-containing cyanobacteria, but in contrast, each photosystem uses Chl d as the main photosynthetic pigment, including the special chlorophyll pairs in both their RCs [50]. The light-harvesting antenna of A. marina is a special Pcb-protein of ca. 34 kDa incorporated by Chl d in concert with some part of Chl a, indicating that this membrane antenna is similar to the Chl a/b-protein of prochlorophytes [51]. Pcb-proteins encircle in the form of a ring the PS II dimers, but data on Pcb composition and function in PS I are currently absent. In summary, Chl d can account for ~95% of total Chls (a + d) in the contents of PS I and PS II [52].
All the known strains of Acaryochloris are free from phycobiliproteins except the first described and most extensively studied “under ascidian niche found” A. marina MBIC11017. Classic cyanobacterial PBSs in this strain are eliminated. Instead, A. marina MBIC11017 contains the rod-shaped phycobiliprotein aggregates located on the cytoplasmic side of the thylakoid membranes along with the intrinsic membrane Pcb-antenna. Each rod is composed of four phycobiliprotein hexamers equal in size to lateral rods in a typical PBS from other cyanobacteria. Rods consist of PC (αβ)6-hexamers with some admixture of pigment, whose absorption spectrum resembles that of APC. The complete chromosome sequence of A. marina demonstrates that, along with PC-related genes, only the apcB gene is present for coding the β-chain of APC, while the corresponding apcA is absent [52]. This means that very unusual (αβ)1-heteromonomers mixed from α-PC and β-APC polypeptides most likely compose the last trimer in the bottom hexamer of a cylinder adjoining the outer thylakoid membrane surface. The presence of both PC and APC, however, within one hexamer seems to be a unique feature of the phycobiliprotein aggregates in A. marina.
The architecture of native cylindrical phycobiliprotein aggregates is much less complex than that of complete PBS. However, the energy transfer to Chl d is very efficient and takes about 70 ps [53]. In isolated preparations [54][55] and in photosynthetic action spectra [56], it has been found that the biliproteins are physically attached to the PS II complexes. Comparison of the surface areas for the rounded bottom of phycobiliprotein cylinders and PS II shows that each PSII dimer can anchor one or two cylinders. Currently, it is not clear whether such an attachment needs special linker protein(s) or not. Due to the cytoplasmic surface area of the PS II dimer [22], there is enough place for the ends of two cylinders. Dimers of PS II in A. marina are paired in tetramers [50]. As a consequence, the phycobiliproteins form separate patches on the thylakoid surface that, highly probably, consist of four cylinders feeding by absorbed energy these PS II tetramers.
Complete sequencing of the Acariochloris genome showed that phycobiliprotein genes are not located in the chromosome but in large cell plasmids. This led to the conclusion that genes for PBS appear to have been previously lost in the common ancestor of Acaryochloris and some other marine cyanobacteria. A. marina MBIC11017 is the only Acaryochloris strain which is thought to have reacquired a set of the phycobiliprotein genes via horizontal gene transport [57].

2.3. Chlorophyll f-Containing Cyanobacteria and Their Involvement in the Process of Photoacclimation to Far Red Light

Chl f was discovered as a minor pigment in a filamentous cyanobacterium Halomicronema hongdechloris collected from living columnar marine stromatolites [34] and has since been found in a number of other cyanobacteria, both filamentous and uni-cellular, including terrestrial species [58]. Compared to A. marina, Chl f-containing cyanobacteria can photosynthesize further into the far-red and near-infrared regions (Chl f gains enhanced absorbance by up to 800 nm) [59]. The amount of Chl f in white light is very small or absent  [60], and its biosynthesis is induced only under FaRLiP (far-red light photoacclimation) conditions. In contrast to Chl d in A. marina, it was shown that Chl f is not part of a special pair in both RCs and functions only in a light-harvesting role in the core antennae of PS I and PS II. The precise cryo-EM data have shown that the FaRLip-PS II pigment–protein complex from Synechococcus sp. PCC 7335 binds one Chl d and four Chl f in place of several of 35 Chl a molecules present in PS II when grown in visible light [61]. Analogously, the high-resolution structure of the far-red PS I core from H. hongdechloris showed that in far-red light, it binds 83 Chl a plus 7 Chl f associated at the periphery of the PS I core antenna [62]. Simultaneously with these pigment replacements, several polypeptide subunits of PS I and PS II cores are remodeled using subunits paralogous to those produced in white light [61][62]. In doing so, even then Chl f constitutes only a small part (less than 10%) of the remaining predominant Chl a but expands the spectral region of solar light absorption.
The architecture of PBS from Leptolyngbia sp. strain JSC-1 exhibits an extensive response to growth in far-red light simultaneously with the stimulation of Chl f biosynthesis. The hemidiscoidal pentacylindrical PBS of this species corresponds to the one of varities of chromatic adaptation synthesizing PE in green and white light and the PC only under red light conditions. In far-red light, the PBS core diminishes to only two APC cylinders, retains PE disks in lateral cylinders while absent in red light, and produces another ApcE linker (ApcE2 instead of ApcE1) with noncovalently bound terminal phycobilin chromophor [59]. This long-wavelength-shifted terminal chromophore better corresponds to effective energy transfer from PBS to Chl f-modified complexes of PS I and PS II. It has been suggested that apcE2 could be used as a marker of FARLiP adaptability in different tested species of cyanobacteria [63]. The genome of Leptolyngbya sp. JCC-1 has a 21-gene cluster that encodes paralogues of most of the core polypeptides of PS I, PS II, and PBSs; similar clusters are found in other FaRLiP-cyanobacteria [59]. All photoacclimation processes usually take approximately one day. The restructured pigment apparatus (i.e., PS I, PS II, PBS) acquires the ability to absorb at longer light wavelengths, which enables cyanobacteria to grow photoautotrophically in far-red light.
To summarize somewhat, it is stated that changes in the composition of phycobiliproteins occur differently in cyanobacteria possessing various kinds of Chl pigments. The vast majority of cyanobacterial species contain only chl a, and the form of their phycobiliprotein antenna is phycobilisomes, which can exist in several morphological variants. There is a complete loss of PBSs and phycobiliproteins in Chl b-containing phototrophs, a reduction from whole PBS to phycobiliprotein cylinders in Chl d-containing species, and only a partial rearrangement of the PBS core and replacement of individual phycobiliproteins in Chl f-containing cyanobacterial cells.

References

  1. Schirrmeister, B.E.; Gugger, M.; Donoghue, P.C.J. Cyanobacteria and the great oxidation event: Evidence from genes and fossil. Paleontology 2015, 58, 769–785, doi.org/10.1111/pala.12178.
  2. Yutin, N.; Wolf, M.Y.; Wolf, Y.I.; Koonin, E.V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 2009, 4, 9, -, 10.1186/1745-6150-4-9..
  3. Martijn, J.; Vosseberg, J.; Guy, L.; Offre, P.; Ettema, T.J.G. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 2018, 557, 101–105, 10.1038/s41586-018-0059-5.
  4. López-Garcìa, P.; Moreira, D. The syntrophy hypothesis for the origin of eukaryotes revisited. Nat. Microbiol. 2020, 5, 655–667, 10.1038/s41564-020-0710-4.
  5. Stadnichuk, I.N.; Kusnetsov, V.V. Endosymbiotic origin of chloroplasts in plant cells evolution. Rus. J. Plant Physiol. 2021, 68, 1–16, 10.1134/S1021443721010179.
  6. Archibald, J.M. Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 2015, 25, R911–R921, 10.1016/j.cub.2015.07.055.
  7. Bhattacharya, D.; Qiu, H.; Lee, J.M.; Yoon, H.S.; Weber, A.P.N.; Price, D.C. When less is more: Red algae as models for stud-ying gene loss and genome evolution in eukaryotes. Crit. Rev. Plant Sci. 2018, 37, 81–99, 10.1080/07352689.2018.1482364.
  8. Figueroa-Martinez, F.; Christopher, J.; Reyes-Prieto, A. Plastid genomes from diverse Glaucophytegenera reveal a largely conserved gene content and limited architectural diversity. Genome Biol. Evol. 2019, 11, 174–188, 10.1093/gbe/evy268.
  9. Donoghue, P.; Paps, J. Plant evolution: Assembling land plants. Curr. Biol. 2020, 30, R81–R83 , 10.1016/j.cub.2019.11.08.
  10. Cavalier-Smith, T. Kingdom Chromista and its eight phyla: A new synthesis emphasising periplastid protein targeting, cyto-skeletal and periplastid evolution, and ancient divergences. Protoplasma 2018, 255, 297–357, 10.1007/s00709-017-1147-3.
  11. Stadnichuk, I.N. Phycobiliproteins: Determination of chromophore composition and content. Phytochem. Analysis 1995, 6, 281–288., 10.1002/pca.2800060602.
  12. Stadnichuk, I.N.; Tropin, I.V. Phycobiliproteins: Structure, functions and biotechnological applications. Appl. Biochem. Microbiol. 2017, 53, 1–10., 10.1006/jmbi.2001.5030.
  13. Betz, M. One century of protein crystallography: The phycobiliproteins. Biol. Chem. 1997, 378, 167–176., 10.1006/jmbi.2001.5030.
  14. Blot, N.; Wu, X.-J.; Thomas, J.-C.; Zhang, J.; Garczarek, L.; Böhm, S.; Tu, J.-M.; Zhou, M.; Plöscher, M.; Eichacker, L.; et al.et al. Phycourobilin in trichromatic phycocyanin from oceanic cyanobacteria is formed post-translationally by a phycoerythrobilin lyase-isomerase. J. Biol. Chem. 2009, 284, 9290–9298, 10.1074/jbc.M809784200.
  15. Bernát, G.; Schreiber, U.; Sendtko, E.; Stadnichuk, I.N.; Rexroth, S.; Rögner, M.; Koenig, F. Unique properties vs. common themes: The atypical cyanobacterium Gloeobacter violaceus PCC 7421 is capable of state transitions and blue-light induced fluorescence quenching. Plant Cell Physiol. 2012, 53, 528–542., 10.1093/pcp/pcs009.
  16. Kondo, K.; Ochiai, Y.; Katayama, M.; Ikeuchi, M. The membrane-associated CpcG2-phycobilisome in Synechocystis: A new photosystem I antenna.. Plant Physiol. 2007, 144, 1200–1210., 10.1104/pp.107.099267.
  17. Elanskaya, I.V.; Zlenko, D.V.; Lukashev, E.P.; Suzina, N.E.; Kononova, I.A.; Stadnichuk, I.N. Phycobilisomes from the mutant cyanobacterium Synechocystis sp. PCC 6803 missing chromophore domain of ApcE. Biochim. Biophys. Acta (BBA)-Bioenerg. 2018, 1859, 280–291, 10.1016/j.bbabio.2018.01.003.
  18. Grébert, T.; Garczarek, L.; Daubin, V.; Humily, F.; Marie, D.; Ratin, M.; Devailly, A.; Farrant, G.K.; Mary, I.; Mella-Flores, D.; et al.et al. Diversity and evolution of pigment types in marine Synechococcus cyanobacteria. Genome Biol. Evol. 2022, 14, evac035, -, 10.1093/gbe/evac035.
  19. Gindt, Y.M.; Zhou, J.; Bryant, D.A.; Sauer, K. Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: Assignment of excited state energies to the Lcm, 18 and AP-B chromophores. Biochim. Biophys. Acta (BBA)- Bioenerg. 1994, 1186, 153–162, 10.1016/0005-2728(94)90174-0.
  20. Dong, C.; Tang, A.; Zhao, J.; Mullineaux, C.W.; Shen, G.; Bryant, D.A. ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002.. Biochim. Biophys. Acta 2009, 1787, 1122–1128, 10.1016/j.bbabio.2009.04.007.
  21. Zheng, L.; Zheng, Z.; Li, X.; Wang, G.; Zhang, K.; Wei, P.; Zhao, J.; Ga, N. Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes. Nat. Commun. 2021, 2, 5497, -, 10.1038/s41467-021-25813-y.
  22. Bald, D.; Kruip, J.; Rögner, M. Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems? . Photosynth. Res. 1996, 49, 103–118, 10.1007/BF00117661.
  23. Rakhimberdieva, M.G.; Boichenko, V.A.; Karapetyan, N.V.; Stadnichuk, I.N. Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry 2001, 40, 15780–15788, 10.1021/bi010009t.
  24. Bryant, D.A.; Canniffe, D.P. How nature designs light-harvesting antenna systems: Design principles and functional realization in chlorophototrophic prokaryotes. J. Phys. B At. Mol. Opt. Phys. 2018, 51, 033001, -, 10.1088/1361-6455/aa9c3c.
  25. Arteni, A.A.; Ajlani, G.; Boekema, E.J. Structural organization of phycobilisomes from Synechocystis strain PCC 6803 and their interaction with the membrane. Biochim. Biophys. Acta 2009, 1787, 272–279, 10.1016/j.bbabio.2009.01.009.
  26. Chang, L.; Liu, X.; Li, Y.; Liu, C.; Yang, F. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 2015, 25, 726–737, 10.1038/cr.2015.59.
  27. Chitnis, V.; Chitnis, P. Psal subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 1993, 336, 330–334, 10.1016/0014-5793(93)80831-E.
  28. Kruip, J.; Chitnis, P.; Lagoutte, B.; Rögner, M.; Boekema, E. Structural organization of the major subunits in cyanobacterial photosystem I. Localization of subunits PsaC, -D, -E, -F, and –J. J. . Biol. Chem. 1997, 272, 17061–17069, 10.1016/0014-5793(93)80831-E.
  29. Zlenko, D.V.; Krasilnikov, P.M.; Stadnichuk, I.N. Structural modeling of the phycobilisome core and its association with the photosystems. Photosynth. Res. 2016, 130, 347–356., 10.1007/s11120-016-0264-8..
  30. Burger-Wiersma, T.; Post, A.F. Functional Analysis of the photosynthetic apparatus of Prochlorothrix hollandica (Prochlorales), a chlorophyll b containing procaryote. Plant Physiol. 1989, 91, 770–774, 10.1104/pp.91.2.770.
  31. Averina, S.G.; Velichko, N.V.; Pinevich, A.A.; Senatskaya, E.V.; Pinevich, A.V. Non-a chlorophylls in cyanobacteria. Photosynthetica 2019, 57, 1109–1118, 10.32615/ps.2019.130.
  32. Lewin, R.A. A marine Synechocystis (Cyanophyta, Chroococcales) epizoic on ascidians. Phycologia 1975, 14, 153–160, 10.2216/i0031-8884-14-3-153.1.
  33. La Roche, J.; Van der Staay, G.; Partensky, F.; Ducret, A.; Aebersold, R.; Li, R.; Golden, S.S.; Hiller, R.; Wrench, P.M.; Larkum, A.W.D.; et al.et al. Independent evolution of the prochlorophyte and green plant chlorophyll a/b light harvesting proteins. Proc. Natl. Acad. Sci. USA 1996, 93, 15244–15248, 10.1073/pnas.93.26.15244.
  34. Chen, M.; Li, Y.Q.; Birch, D.; Willows, R.D. A cyanobacterium that contains chlorophyll f -a red-absorbing photopigment. FEBS Lett. 2012, 586, 3249–3254, 10.1016/j.febslet.2012.06.045.
  35. Giddings, T.H., Jr.; Withers, N.W.; Staehelin, L.A. Supramolecular structure of stacked and unstacked regions of the photosynthetic membranes of Prochloron sp., a prokaryote. Proc. Natl. Acad. Sci. USA 1980, 77, 352–356, 10.1073/pnas.77.1.352.
  36. Boichenko, V.A.; Pinevich, A.V.; Stadnichuk, I.N. Association of chlorophyll a/b-binding Pcb proteins with photosystems I and II in Prochlorothrix hollandica. Biochim. Biophys. Acta (BBA)-Bioenerg. 2007, 1767, 801–806, 10.1016/j.bbabio.2006.11.001.
  37. Barrera-Rojas, J.; González de la Vara, L.E.; Ríos-Castro, E. The distribution of divinyl chlorophylls a and b and the presence of ferredoxin-NADP+ reductase in Prochlorococcus marinus MIT9313 thylakoid membranes. Helion 2018, 4, e01100, -, 10.1016/j.heliyon.2018.e01100.
  38. Larkum, A.W.D.; Scaramuzzi, C.; Cox, G.C.; Hiller, R.G.; Turner, A.G. Light harvesting chlorophyll c-like pigment in Prochloron. Proc. Natl. Acad. Sci. USA 1994, 91, 678–683, 10.1073/pnas.91.2.679.
  39. Hess, W.R.; Partensky, F.; Van der Staay, G.W.M.; Garcia-Fernandez, J.M.; Börner, T.; Vaulot, D. Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc. Natl. Acad. Sci. USA 1996, 93, 11126–11130, 10.1073/pnas.93.20.11126.
  40. Penno, S.; Campbell, L.; Hess, W.R. Presence of phycoerythrin in two strains of Prochlorococcus isolated from the sub-tropical North Pacific Ocean. J. Phycol. 2000, 36, 723–729, 10.1046/j.1529-8817.2000.99203.x.
  41. Beale, S.I. Photosynthetic pigments: Perplexing persistent prevalence of ‘superfluous’ pigment production. Curr. Biol. 2008, 18, R342–R343., 10.1016/j.cub.2008.02.064.
  42. Moore, L.R.; Rocap, G.; Chisholm, S.W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 1998, 393, 464–467, 10.1038/30965.
  43. Wiethaus, J.; Busch, A.W.U.; Dammeyer, T.; Frankenberg-Dinkel, N. Phycobiliproteins in Prochlorococcus marinus: Biosynthesis of pigments and their assembly into proteins. Eur. J. Cell Biol. 2010, 89, 1005–1010, 10.1016/j.ejcb.2010.06.017.
  44. Hess, W.R.; Steglich, C.; Lichtlé, C.; Partensky, F. Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol. Biol. 1999, 40, 507–521, 10.1023/a:1006252013008.
  45. Ting, C.S.; Rocap, G.; King, J.; Chisholm, S.W. Phycobiliprotein genes of the marine photosynthetic prokaryote Prochlorococcus: Evidence for rapid evolution of genetic heterogeneity. Microbiology 2001, 147, 3171–3182, 10.1099/00221287-147-11-3171.
  46. Sonani, R.R.; Rastogi, R.P.; Joshi, M.; Madamwar, D. A stable and functional single peptide phycoerythrin (15.45 kDa) from Lyngbya sp. A09DM. Int. J. Biol. Macromol. 2015, 74, 29–35., 10.1016/j.ijbiomac.2014.11.030.
  47. Ikeuchi, M.; Ishizuka, T. Cyanobacteriochromes: A new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 2008, 7, 1159–1167, 10.1039/b802660m.
  48. Miyashita, H.; Ikemoto, H.; Kurano, N.; Adachi, K.; Chihara, M.; Miyachi, S. Chlorophyll d as a major pigment. Nature 1996, 383, 402, -, 10.1038/383402a0.
  49. Miller, S.R.; Abresch, H.E.; Baroch, J.J.; Miller, C.K.F.; Garber, A.I.; Oman, A.R.; Ulrich, N.J. Genomic and functional variation of the chlorophyll d-producing cyanobacterium Acaryochloris marina. Microorganisms 2022, 10, 569, -, 10.3390/microorganisms10030569.
  50. Tomo, T.; Okubo, T.; Akimoto, S.; Yokono, M.; Miyashita, H.; Tsuchiya, T.; Noguchi, T.; Mimuro, M. Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc. Natl. Acad. Sci. USA 2007, 104, 7283–7288, 10.1073/pnas.070184710.
  51. Chen, M.; Quinnell, R.G.; Larkum, A.W.D. The major light-harvesting pigment protein of Acaryochloris marina. FEBS Lett. 2002, 514, 149–152, 10.1016/s0014-5793(02)02315-3.
  52. Yamamoto, H.; Uesaka, K.; Tsuzuki, Y.; Yamakawa, H.; Itoh, S.; Fujita, Y. Comparative genomic analysis of the marine cyanobacterium Acaryochloris marina MBIC10699 reveals the impact of phycobiliprotein reacquisition and the diversity of Acaryochloris plasmids. Microorganisms 2022, 10, 1`374, -, 10.3390/microorganisms10071374.
  53. Theiss, C.; Schmitt, F.-J.; Pieper, J.; Nganou, C.; Grehna, M.; Vitali, M.; Olliges, R.; Eichler, H.J.; Eckert, H.-J. Excitation energy transfer in intact cells and in the phycobiliprotein antennae of the chlorophyll d containing cyanobacterium Acaryochloris marina. J. Plant Physiol. 2011, 168, 1473–1487, 10.1016/j.jplph.2011.02.002.
  54. Marquardt, J.; Senger, H.; Miyashita, H.; Miyachi, S.; Mörschel, E. Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett. 1997, 410, 428–432., 10.1016/s0014-5793(97)00631-5.
  55. Hu, Q.; Marquardt, J.; Iwasaki, I.; Miyashita, H.; Kurano, N.; Mörschel, E.; Miyachi, S. Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochim. Biophys. Acta 1999, 1412, 250–261, 10.1016/s0005-2728(99)00067-5.
  56. Boichenko, V.A.; Klimov, V.V.; Miyashita, H.; Miyachi, S. Functional characteristics of chlorophyll d-predominating photosynthetic apparatus in intact cells of Acaryochloris marina. Photosynth. Res. 2000, 65, 269–277, 10.1023/A:1010637631417.
  57. Ulrich, N.J.; Uchida, H.; Kanesaki, Y.; Hirose, E.; Murakami, A.; Miller, S.R. Reacquisition of light-harvesting genes in a marine cyanobacterium confers a broader solar niche. Curr. Biol. 2021, 31, 1539–1546., 10.1016/j.cub.2021.01.047.
  58. Ho, M.-Y.; Soulier, N.T.; Canniffe, D.P.; Shen, G.; Bryant, D.A. Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr. Opin. Plant Biol. 2017, 37, 24–33, 10.1016/j.pbi.2017.03.006.
  59. Gan, F.; Zhang, S.; Rockwell, N.C.; Martin, S.S.; Lagarias, J.C.; Bryant, D.A. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 2014, 345, 1312–1317, 10.1126/science.1256963.
  60. Larkum, A.W.D.; Ritchie, R.J.; Raven, J.A. Living off the Sun: Chlorophylls, bacteriochlorophylls and rhodopsins. Photosynthetica 2018, 56, 11–43, 10.1007/s11099-018-0792-x.
  61. Gisriel, C.J.; Shen, G.; Ho, M.-Y.; Kurashov, V.; Fleshe, D.A.; Wang, J.; Armstrong,W.H.; Golbeck, J.H.; Gunner, M.R.; Vinyard, D.J.; et al.et al. Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red light reveals the functions of chlorophylls d and f. J. Biol. Chem. 2022, 298, 101424, -, 10.1016/j.jbc.2021.101424.
  62. Kato, K.; Shinoda, T.; Nagao, R.; Akimoto, S.; Suzuki, T.; Dohmae, N.; Chen, M.; Allakhverdiev, S.I.; Shen, J.-R.; Akita, F.; et al.et al. Structural basis for the adaptation and function of chlorophyll f in photosystem I. Nat. Commun. 2020, 11, 238, -, 10.1038/s41467-019-13898-5 .
  63. Antonaru, L.A.; Cardona, T.; Larkum, A.W.D.; Nürnberg, D.J. Global distribution of a chlorophyll f cyanobacterial marker. ISME J. 2020, 14, 2275–2287, 10.1038/s41396-020-0670-y .
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Biochemistry & Molecular Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Igor N. Stadnichuk
,
Victor V. Kusnetsov
View Times: 1.1K
Revisions: 2 times (View History)
Update Date: 14 Feb 2023
Table of Contents
    1000/1000
    Hot Most Recent
    Academic Video Service
    Feedback