Cyanobacteria, also known as blue–green algae, are ubiquitous organisms on the planet. They contain tremendous protein machineries that are of interest to the biotechnology industry and beyond. Recently, the number of annotated cyanobacterial genomes has expanded, enabling structural studies on known gene-coded proteins to accelerate. This review focuses on the advances in mass spectrometry (MS) that have enabled structural proteomics studies to be performed on the proteins and protein complexes within cyanobacteria. The review also showcases examples whereby MS has revealed critical mechanistic information behind how these remarkable machines within cyanobacteria function.

Cyanobacteria, also known as blue–green algae, are among the oldest and most populous organisms on the planet. They have great potential in applications in biotechnology [1–3] including biofuel production [4], colorants [5,6], dietary supplements [7] and wastewater treatment [8,9]. Moreover, cyanobacteria can produce bioactive compounds with antiviral [10], anticancerous [11], antifungal [12] and antibacterial [13] activity making them an attractive research area. Understanding the genetic composition, the proteins cyanobacteria produce and how these function are important to fully exploit their biotechnological potential.

Until the early 2000s, obtaining cyanobacterial genome sequences was challenging due to the strong symbiotic relationship of cyanobacteria with other organisms and the strict requirement for axenic cultures for effective genome sequencing [14–16]. In addition, complications can arise since cyanobacteria can create disorder in their genome through horizontal gene transfer [17] when they adapt to new environments. Thus, even by 2017, the number of cyanobacterial genomic sequences was still relatively low compared with other bacterial phyla [18]. However, recent advances in metagenomics [18] that circumvent the need for axenic cultures are transitioning this research area and consequently the numbers of sequenced cyanobacterial genomes are now expanding rapidly. Alongside these developments, eDNA metabarcoding is providing a potentially highly effective approach for routine monitoring of cyanobacteria within cyanobacterial blooms [19,20].

Simultaneous to these developments, the field of cyanobacterial proteomics has also been expanding rapidly [21–24]. With developments in high resolution mass spectrometers that operate at high sensitivity, hundreds of proteins within cyanobacteria can effectively be screened to determine how cyanobacteria respond or adapt to environmental stimuli [25–27]. Moreover, now encoded protein sequences are available, structural biology experiments have begun to investigate the encoded proteins’ functional proteoform(s). This review will focus on these recent advances in structural proteomics and how the application of this technology has accelerated our in-depth understanding of the remarkable cellular processes within cyanobacteria.

Despite the focus of this review being proteomics, it is important that the integration of genomics and proteomics and the parallel advancement of both techniques continues. Indeed, due to the complexity of cyanobacterial genetic analysis, mistakes can occur within genome sequences that can subsequently be ‘corrected’ through proteomic analysis. For example, a proteogenomics study by Zhao and co-workers was able to correct 38 predicted gene-coding regions of the Synechococcus sp. PCC 7002 genome [28]. Single amino acid differences at the individual protein level have also been noted upon proteomic analysis. For example, the discrepancy between an arginine or alanine residue at position 21 in the β-subunit of allophycocyanin in Arthrospira platensis was confirmed using mass spectrometry (MS) to be alanine [29,30]. Indeed, through MS-based protein sequencing the predominant protein, phycocyanin, within the light harvesting complex of Phormidium rubidium was found to have 49 differences compared with its gene-derived sequence, which ultimately led to a more precise structure of its resulting complex [31]. Moreover, it is only with the knowledge of correct protein sequences within the cyanobacterial genome that we can perform structural studies to capture the details of how proteins and protein complexes function at the molecular level.

Structural proteomics is the analysis of 3D protein structures with the aim to understand how proteins function on a genome-wide scale [32,33]. Traditionally, structural biology has focused on individual proteins or protein complexes with the aim to build mechanistic information about how they operate. Exciting bioinformatic developments in AlphaFold [34], mean protein structures can now largely be predicted from their primary sequence. Cryo-electron microscopy, in particular single particle cryo-electron microscopy, has overcome a major barrier in solving structures of large assemblies, being able to provide snapshots of complexes at atomic resolution [35,36]. However, alternative techniques are still required to fully capture protein dynamics and transient interactions, together with the large heterogeneity that is present within some functional complexes. Moreover, the structures of protein complexes can be challenging to predict, and we still rely on biophysical measurements to fully characterise their interactions. Additional complexity also occurs when proteins are dynamically modified with PTMs that themselves create heterogeneity within complexes and can drastically alter a protein’s function. It is to this end that structural MS can be advantageous.

MS alone, whereby a protein is infused directly into a mass spectrometer, has provided a wealth of information on protein structures within cyanobacteria (Figure 1). Through intact mass measurements, protein oligomeric states can be discerned, binding stoichiometry determined between proteins and ligands, and the extent and nature of any PTMs deciphered [37–39]. Tandem MS (MS/MS) on proteins or protein complexes provides additional information on protein stability and protein complex topology [40,41]. In combination with ion mobility spectrometry, the conformation of proteins and protein complexes can be revealed [42–44]. These aforementioned techniques encompass the basis of native MS whereby structural information is inferred by analyzing protein or protein complexes in as close conditions as possible to their cellular environment [38,45]. MS can also be used to map sites within protein interaction interfaces. Protein footprinting techniques, including most commonly used hydrogen deuterium exchange [46,47] and hydroxyl radical footprinting [48,49], can be used to probe in-solution differences in backbone interactions and side chain solvent accessibility, respectively, between different protein states. Within the gas-phase in the mass spectrometer, top-down fragmentation can additionally probe B factor or surface residues that reveal information on binding interactions and protein conformational states [50]. In addition, cross-linking provides a means to capture transient complexes or conformational states prior to MS analysis. By cross-linking amino acid side chains in close proximity and monitoring these sites of modification, structural constraints can be placed on proteins or protein complexes that enable models to be built or static structures to be re-evaluated [51–53]. Moreover, with on-going developments in online separation techniques (e.g. size exclusion chromatography) and data analysis tools, the wealth of information structural MS provides within a single study is being expanded beyond the single protein complex level towards deciphering the dynamics of hundreds of endogenous protein complexes [54]. Furthermore, since MS separates by mass-to-charge ratio, different protein proteoforms can be separated and the heterogeneity within complexes visualized [55], thus, showcasing how MS can be advantageous over other structural biology techniques. A summary of the types of information structural MS can provide are highlighted in Figure 1, pointing to exemplar studies of how each technique has been applied within cyanobacteria. In the next sections, we expand on the insight these techniques have brought to our understanding of PTMs and protein complex topologies within cyanobacteria, that together have built our knowledge on how key complexes within cyanobacteria function.

Structural information provided by MS

Figure 1
Structural information provided by MS

The figure showcases how structural MS can provide information on oligomeric states and complex topology [56,57], protein–ligand or protein–metal interactions [58] and protein conformations [59] through native MS. PTMs can be determined through intact mass [60] combined with bottom-up and top-down approaches [61] with cross-linking MS [62] and protein footprinting [63] revealing information about transient interactions and protein binding interfaces.

Figure 1
Structural information provided by MS

The figure showcases how structural MS can provide information on oligomeric states and complex topology [56,57], protein–ligand or protein–metal interactions [58] and protein conformations [59] through native MS. PTMs can be determined through intact mass [60] combined with bottom-up and top-down approaches [61] with cross-linking MS [62] and protein footprinting [63] revealing information about transient interactions and protein binding interfaces.

Close modal

MS excels in its ability to resolve minor mass differences on intact proteins and thus can distinguish many protein proteoforms. Through MS/MS experiments, the sites of PTMs can be localised and their abundance quantified [64–67]. These advantages of MS in PTM identification have meant that many PTMs, which play major roles in many physiological processes within cyanobacteria, have now been reported. Indeed, it is the PTM of phycobiliproteins with phycocyanobilins that provides cyanobacteria with their characteristic blue–green colour. These phycocyanobilin PTMs are essential to light harvesting and energy transfer within cyanobacteria’s photosynthetic machinery. Moreover, proteins that contain phycocyanobilins have been biotechnologically exploited for use as fluorescent probes [68–70], food colourants [71–73] and in cosmetics [74,75] due to their remarkable blue colour. However, PTMs are not confined to light harvesting complexes. Other essential processes within cyanobacteria that also heavily rely on PTMs include: nitrogen fixation [76,77], photosynthesis [78–84], thermal adaptation [85,86], chromatic adaptation [87–89], carbon/nitrogen control [90–94] and circadian rhythm [95–99] (Figure 2).

Selected protein PTMs that occur in cyanobacteria

Figure 2
Selected protein PTMs that occur in cyanobacteria

Seven key PTMs are highlighted including methylation, phosphorylation, chromophorylation, glutationylation, lipidation, propionylation and acetylation that collectively play roles in circadian rhythm, nitrogen fixation, photosynthesis and thermal adaptation. The protein side chains and PTM structures are shown in black and green, respectively.

Figure 2
Selected protein PTMs that occur in cyanobacteria

Seven key PTMs are highlighted including methylation, phosphorylation, chromophorylation, glutationylation, lipidation, propionylation and acetylation that collectively play roles in circadian rhythm, nitrogen fixation, photosynthesis and thermal adaptation. The protein side chains and PTM structures are shown in black and green, respectively.

Close modal

Overall, MS analysis of cyanobacterial proteins has identified several types of PTMs. For instance, proteomic studies determined 23 and 27 different types of PTM in Synechococcus sp. PCC 7002 [28] and Nostoc sp. PCC 7120 [100], respectively, using MS. These PTMs in cyanobacteria include, but are not limited to, phosphorylation [25,101–107], acetylation [60,108,109], glutathionylation [110], lipidation [111,112], propionylation [113,114], malonylation [115], methylation [82,83], succinylation [116,117] and glycosylation [118] as illustrated in Figure 2. The presence of these modifications can directly impact cellular processes. For example, the phosphorylation of Ser-49 of the PII signal transduction protein is an important factor in signalling nitrogen deficiency [25,91,93], while the acetylation of K-190 of the protein PsbO is involved in the negative regulation of oxygen evolution in photosystem II [109]. Another notable example is on RexT, a redox-sensing transcriptional regulator, whereby MS helped locate Cys-41 as a critical cysteine residue that forms a vicinal disulphide bond in response to elevated hydrogen peroxide levels [119].

Another prominent example of PTMs in cyanobacteria is in controlling circadian rhythm. Within this, KaiC undergoes autophosphorylation, KaiA enhances autophosphorylation of KaiC, while KaiB antagonises it [96–98]. Moreover, phosphorylation of KaiC follows a four-step sequence whereby: (1) Thr-432 is phosphorylated, (2) Ser-431 is phosphorylated, (3) Thr-432 is dephosphorylated, and (4) Ser-431 is dephosphorylated, resulting in the non-phosphorylated form of KaiC which can subsequently restart the sequence [120,121] (Figure 3A). It is these oscillating levels of phosphorylation and dephosphorylation of KaiC that are essential for determining the phase of circadian rhythm [99,122,123]. The importance of PTMs in cyanobacteria is not limited to just the protein level. Cyanobactins, peptides produced as secondary metabolites, are heavily post-translationally modified with both prenylation [124–126] and geranylation [127] modifications reported. The findings of which have been reviewed in more detail elsewhere [128,129].

Schematic of the circadian clock and photosynthetic machinery within cyanobacteria

Figure 3
Schematic of the circadian clock and photosynthetic machinery within cyanobacteria

(A) Schematic of KaiCBA protein complexes that form throughout the circadian cycle as informed by structural proteomics studies. (B) Cartoon images of the six major complexes: PBS, photosystem I and II, cytochrome b6f and ATP synthase are shown alongside plastoquinone (PQ), plastocyanin (Pc) and the OCP.

Figure 3
Schematic of the circadian clock and photosynthetic machinery within cyanobacteria

(A) Schematic of KaiCBA protein complexes that form throughout the circadian cycle as informed by structural proteomics studies. (B) Cartoon images of the six major complexes: PBS, photosystem I and II, cytochrome b6f and ATP synthase are shown alongside plastoquinone (PQ), plastocyanin (Pc) and the OCP.

Close modal

Overall, despite ancestral origin, the different types of PTMs found across cyanobacteria species are vast, with new modifications continuing to be discovered. As the diversity of MS methods to study PTMs evolves (Table 1), our ability to capture and monitor the function of these modifications will expand. We anticipate that the number of detected PTMs will also continue to increase with advancements in higher sensitivity instruments, the development of novel enrichment techniques for PTMs that occur sub-stoichiometrically, and enhanced bioinformatics tools that enable ‘open’ searching of MS/MS data without prior knowledge of the PTM of interest. However, these novel PTMs must be taken with caution, be carefully annotated to avoid mis-interpretation [130], and their presence confirmed in vivo through biological characterisation.

Table 1
MS methods used to identify protein PTMs in cyanobacteria
MS methodPTM information providedExamples of PTMs observed using MS method
Native MS Stoichiometry and nature of PTMs on native protein complexes ● Phosphorylation on KaiC and KaiCBA oligomers [131
  ● Bilin modification and methyl-asparagine on phycobiliprotein hexamers [30,132
Top-down MS Site-localisation and stoichiometry of PTMs on individual proteins ● N-terminal acetylation of PetC within the Cytochrome b6f complex [61
  ● Lipidation of photosystem II assembly factors, Ycf48 [133] and Psb27 [111
  ● Bilin modification on cysteine residues within phycobiliproteins [134
Bottom-up MS Site-localisation of PTMs in a high-throughput approach ● Lysine methylation [135
  ● Phosphorylation on KaiC [136], ET-Tu [137] and PBS proteins [138
  ● Bilin modifications on phycobiliproteins [139
  ● Lysine propionylation (many sites detected in regulation of photosynthesis and metabolism) [113
  ● Glutathionylation of peroxiredoxin and 3-phosphoglycerate dehydrogenase [110
  ● C-terminal processing of D1 in photosystem II [140
MS methodPTM information providedExamples of PTMs observed using MS method
Native MS Stoichiometry and nature of PTMs on native protein complexes ● Phosphorylation on KaiC and KaiCBA oligomers [131
  ● Bilin modification and methyl-asparagine on phycobiliprotein hexamers [30,132
Top-down MS Site-localisation and stoichiometry of PTMs on individual proteins ● N-terminal acetylation of PetC within the Cytochrome b6f complex [61
  ● Lipidation of photosystem II assembly factors, Ycf48 [133] and Psb27 [111
  ● Bilin modification on cysteine residues within phycobiliproteins [134
Bottom-up MS Site-localisation of PTMs in a high-throughput approach ● Lysine methylation [135
  ● Phosphorylation on KaiC [136], ET-Tu [137] and PBS proteins [138
  ● Bilin modifications on phycobiliproteins [139
  ● Lysine propionylation (many sites detected in regulation of photosynthesis and metabolism) [113
  ● Glutathionylation of peroxiredoxin and 3-phosphoglycerate dehydrogenase [110
  ● C-terminal processing of D1 in photosystem II [140

MS studies on cyanobacteria have led to the identification of novel protein complexes that are dependent upon the cyanobacteria’s cellular context. These findings have often been a result of looking at intact protein complexes rather than individual proteins. Indeed, if a novel protein is detected within a macromolecular complex of known function, this on its own provides functional insight into the role of the newly identified protein, which may alter in response to cellular stimuli. Moreover, a study by Guerreiro et al. noted that when looking at global protein levels, the fluctuation in proteins in response to light was not very pronounced [141]. However, when native protein complex fractionation (size exclusion chromatography) was combined with high resolution proteomics, large complex assemblies including ribosomal and photosynthetic complexes were observed to change in response to light [57]. Within these data, more component variety was observed within photosynthetic complexes in the light phase, a finding that would be undetectable at the individual protein analysis level. In another light-dependent study, through pull-down experiments followed by MS analysis, a collection of proteins that are directly or indirectly associated with the vesicle-inducing protein in plastid 1 (Vipp1) were identified only after exposure to light suggesting that Vipp1 may be involved in protein assembly [142]. In more recent studies, Xu et al. used a combination of size-exclusion chromatography, ion exchange chromatography and sucrose density gradient centrifugation followed by MS, collectively termed Co-Frac-MS, to map the protein interactome within Synechocystis sp. PCC 6803 revealing new insights into photosynthesis, cell mobility and lipid metabolism [143]. With additional developments in native polyacrylamide gel electrophoresis, these MS studies can now be expanded to the analysis of membrane complexes that are more challenging to analyse by conventional separation techniques [144].

On the structural level, the ability of native MS to monitor oligomeric states of proteins and determine protein complex topology has been utilised to reveal new insight within several protein complexes within cyanobacteria. Hackenberg et al. used native MS to show that the cystathionine β-synthase (CBS)-chloroplast protein (CP12) fusion protein, as a single entity, can form a hexameric structure that has suggested roles in redox regulation [145]. Eisenberg et al. were able to monitor how the oligomeric state of phycocyanin increases with increasing concentration, which might indicate how light harvesting systems adapt to a range of environmental conditions [146]. In addition, elegant studies by Clarke and co-workers have revealed the complex topology of two different Clp proteases, ClpXP1/P2 [147] and ClpP3/R [148], that operate to drive protein substrate unfolding prior to proteolytic degradation.

Other work of note where determining the oligomeric statuses’ of proteins has been advantageous is centred around the carboxysome; the compartments within cyanobacteria that are responsible for fixing carbon from inorganic substances [149]. The assembly of the carboxysome shell follows a complex series of events. Garcia-Alles et al. showed CcmK can assemble into hexameric structures [150] with some isoforms forming higher order structures that are dynamic in nature [151]. These CcmK assemblies then further aggregate to form the faces of the carboxysome. Inside the carboxysome reside the enzymes ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase that together act to fix carbon dioxide. Native MS in combination with size exclusion chromatography coupled to right-angled light scattering showed that the small domains within CcmM, a protein involved in RuBisCO recruitment to the β-carboxysome, bind independently of the RbcS subunit, a small subunit of RuBisCO, suggesting it locates within an extended electronegative pocket between the RbcL dimers of RuBisCO, contrary to previously predicted interactions [152]. In another study on RuBisCO, its metabolic repair mechanism by the AAA+ chaperone RuBisCO activase (Rca) was investigated [153]. Native MS confirmed the stable hexameric state of the engineered Rca complex which, using a combination of hydrogen-deuterium exchange MS, cross-linking MS and cryo-electron microscopy, was shown to have conformational effects on RuBisCO’s catalytic site upon interaction [153].

With the increasing developments in structural MS techniques, not only are new proteins and their interaction partners being discovered, but detailed mechanistic information of how key complexes function within cyanobacteria are becoming apparent. Two prominent examples of protein machineries that are noteworthy of further discussion are the circadian clock and photosynthesis.

As mentioned previously, phosphorylation is key in controlling circadian rhythm. In addition to mapping sites of phosphorylation on KaiC [120,121], native MS studies have taken strides in revealing how phosphorylation can alter Kai’s multi-component complexes (Figure 3A). Initial native MS studies into the circadian system showed that KaiB can form monomers, dimers, and tetramers, whereby KaiB binds as a monomer to KaiC in a cooperative fashion to form a KaiC6B6 complex [154]. Following this, native MS was used to prepare well-defined stoichiometric assembles of KaiCB and KaiCBA (specifically KaiC6B6 and KaiC6B6A12) that enabled their structural characterisation by single particle cryo-electron microscopy together with hydrogen-deuterium exchange MS and cross-linking MS [155]. Since then, native MS has further shown that autophosphorylation of hexameric KaiC can promote its binding to dimeric KaiA [156]. These data together provided a structural basis to understand complex assembly within the oscillating clock.

Another area where structural MS is making strides forwards is in our understanding of photosynthesis [157]. There are six major complexes that combine to aid photosynthesis within cyanobacteria: the phycobilisome (PBS), photosystem I and II, cytochrome b6f, NAD(P)H quinone oxidoreductase complex, and ATP synthase (Figure 3B). The PBS is a large light harvesting complex consisting of phycocyanin rods, connected by linker proteins, and an allophycocyanin core. Early work using gentle in vivo cross-linking followed by MS analysis was able to capture weak interactions within the large scale organisation of the PBS and photosystems, showing both photosystem I and II could interact with the PBS [62]. Later cross-linking work was able to predict potential docking interactions between the phycocyanin rods and the allophycocyanin core [158], and suggest a side-view crossover configuration of the two basal cylinders within the PBS core [159]. Furthermore, other studies have shown ferredoxin-NADP+ oxidoreductase, an enzyme involved in electron transport, and non-bleaching protein A, a proteolytic adapter protein, bind phycocyanin to fine-tune energy transfer [160] and PBS degradation [161], respectively. This MS work together combined with the most recent cryo-electron microscopy structures of the PBS [162,163] are aiding significantly in our understanding of how these light harvesting complexes function so efficiently.

When light levels are too high during photosynthesis, protective mechanisms within cyanobacteria must be in place to prevent photodamage. Orange carotenoid protein (OCP) has known photoprotective capabilities and binds to the PBS when light levels are too high [164–166]. Native MS revealed that OCP dimerises to different extents between its active and inactive forms [167]. The conformational differences between the two states have also been probed by footprinting MS [63,168–171]. Using cross-linking MS studies, the N-terminal domain of the active OCP was further found to bury into the PBS, changing the conformation of the allophycocyanin core, resulting in decoupling of light transfer from the PBS towards photosystem II [172,173]. This leaves the C-terminal domain of OCP exposed for binding to the dimeric fluorescence recovery protein that then converts OCP back to its inactive state [169,174]. Like the PBS, photosystem II also needs to be protected from photo-induced damage. Photosystem II is a multi-component protein complex, predominantly composed of reaction centre proteins (D1 and D2), cytochrome b559, and the chlorophyll-containing proteins (CP43 and CP47), that is responsible for water splitting, oxygen evolution and plastoquinone reduction. Two proteins, Psb27 and Psb28, are important in the successful repair of photosystem II [112,175]. A combination of cross-linking MS and protein footprinting MS studies have shown that Psb27 binds CP43 leading to the recruitment other proteins [176–178]. In contrast, Psb28 was found to bind to the CP43-less assembly intermediate known as RC47 [179]. Using an isotope encoded chemical cross-linker and MS, Psb28 was further found to bind to the cytosolic side of cytochrome b559, acting to protect the photosystem II subcomplexes until the photosystem II is ready to function [180].

Together, these MS studies have revealed insight into the PBS, photosystem I and photosystem II within the photosynthetic machinery of cyanobacteria. However, these structural MS studies are only the beginning with the developments in Alphafold 2 now providing more insight into even the intrinsically disordered regions within the PBS that can be further refined using structural MS [181]. We foresee this combined knowledge will accelerate our understanding on how all the photosynthetic complexes within cyanobacteria orchestrate to form the optimal functioning photosynthetic machinery.

Structural proteomics can provide a wealth of information on how proteins function. Within cyanobacteria, structural MS has played a pivotal role in deciphering protein post-translational states, determining protein interaction partners, and revealing mechanistic details behind how proteins function. In this review, we have showcased examples of how structural MS has provided information on circadian rhythm, carbon fixation and photosynthesis. However, we envisage that many macromolecular complexes within cyanobacteria are yet to benefit from structural MS studies, the knowledge of which will significantly advance our understanding of how cyanobacteria function and produce their remarkably efficient protein machines.

  • Cyanobacteria are bursting with biotechnological potential.

  • Advances in structural mass spectrometry are providing great insight into protein proteoforms and their interaction partners that together provide insight into how these function within cyanobacteria.

  • This review highlights examples of where structural mass spectrometry has advanced our knowledge of important molecular mechanisms within cyanobacteria.

The authors declare that there are no competing interests associated with the manuscript.

The work was supported by the BBSRC [grant number BB/T015640/1] and the University of Birmingham funded Midlands Integrative Biosciences Training Partnership (MIBTP2) [grant number BB/S019456/1].

A.C.L. designed the review with input from J.K.S. and J.B.C. on the initial draft. The review was written by J.K.S. and A.C.L. All authors edited the final version of the review.

ATP

adenosine triphosphate

eDNA

environmental DNA

LC

liquid chromatography

MS

mass spectrometry

MS/MS

tandem mass spectrometry

NADPH

nicotinamide adenine dinucleotide phosphate

OCP

orange carotenoid protein

PTM

post-translational modification

RuBisCO

ribulose 1,5-bisphosphate carboxylase/oxygenase

1.
Abed
R.M.M.
,
Dobretsov
S.
and
Sudesh
K.
(
2009
)
Applications of cyanobacteria in biotechnology
.
J. Appl. Microbiol.
106
,
1
12
[PubMed]
2.
Grewe
C.B.
and
Pulz
O.
(
2012
)
The biotechnology of cyanobacteria
. In
Ecology of Cyanobacteria II: Their Diversity in Space and Time
(
Whitton
B.A.
, ed.), pp.
707
739
,
Springer Netherlands
,
Dordrecht
3.
Zahra
Z.
,
Choo
D.H.
,
Lee
H.
and
Parveen
A.
(
2020
)
Cyanobacteria: review of current potentials and applications
.
Environments
7
,
13
4.
Farrokh
P.
,
Sheikhpour
M.
,
Kasaeian
A.
,
Asadi
H.
and
Bavandi
R.
(
2019
)
Cyanobacteria as an eco-friendly resource for biofuel production: a critical review
.
Biotechnol. Prog.
35
,
e2835
[PubMed]
5.
Landim Neves
M.I.
,
Silva
E.K.
and
Meireles
M.A.A.
(
2021
)
Natural blue food colorants: consumer acceptance, current alternatives, trends, challenges, and future strategies
.
Trends Food Sci. Technol.
112
,
163
173
6.
Saini
D.K.
,
Pabbi
S.
and
Shukla
P.
(
2018
)
Cyanobacterial pigments: perspectives and biotechnological approaches
.
Food Chem. Toxicol.
120
,
616
624
[PubMed]
7.
Lafarga
T.
,
Fernández-Sevilla
J.M.
,
González-López
C.
and
Acién-Fernández
F.G.
(
2020
)
Spirulina for the food and functional food industries
.
Food Res. Int.
137
,
109356
[PubMed]
8.
Mehta
S.K.
and
Gaur
J.P.
(
2005
)
Use of algae for removing heavy metal ions from wastewater: progress and prospects
.
Crit. Rev. Biotechnol.
25
,
113
152
[PubMed]
9.
El-Sheekh
M.
,
El-Dalatony
M.M.
,
Thakur
N.
,
Zheng
Y.
and
Salama
E.-S.
(
2022
)
Role of microalgae and cyanobacteria in wastewater treatment: genetic engineering and omics approaches
.
Int. J. Environ. Sci. Technol.
19
,
2173
2194
10.
Mazur-Marzec
H.
,
Cegłowska
M.
,
Konkel
R.
and
Pyrć
K.
(
2021
)
Antiviral cyanometabolites-a review
.
Biomolecules
11
,
474
[PubMed]
11.
Qamar
H.
,
Hussain
K.
,
Soni
A.
,
Khan
A.
,
Hussain
T.
and
Chénais
B.
(
2021
)
Cyanobacteria as natural therapeutics and pharmaceutical potential: role in antitumor activity and as nanovectors
.
Mol. Basel Switz.
26
,
E247
12.
Bertin
M.J.
,
Demirkiran
O.
,
Navarro
G.
,
Moss
N.A.
,
Lee
J.
,
Goldgof
G.M.
et al.
(
2016
)
Kalkipyrone B, a marine cyanobacterial γ-pyrone possessing cytotoxic and anti-fungal activities
.
Phytochemistry
122
,
113
118
[PubMed]
13.
Carpine
R.
and
Sieber
S.
(
2021
)
Antibacterial and antiviral metabolites from cyanobacteria: their application and their impact on human health
.
Curr. Res. Biotechnol.
3
,
65
81
14.
Choi
G.-G.
,
Bae
M.-S.
,
Ahn
C.-Y.
and
Oh
H.-M.
(
2008
)
Induction of axenic culture of arthrospira (spirulina) platensis based on antibiotic sensitivity of contaminating bacteria
.
Biotechnol. Lett
30
,
87
92
[PubMed]
15.
Cornet
L.
,
Meunier
L.
,
Vlierberghe
M.V.
,
Léonard
R.R.
,
Durieu
B.
,
Lara
Y.
et al.
(
2018
)
Consensus assessment of the contamination level of publicly available cyanobacterial genomes
.
PLoS ONE
13
,
e0200323
[PubMed]
16.
Watanabe
M.M.
,
Nakagawa
M.
,
Katagiri
M.
,
Aizawa
K.
,
Hiroki
M.
and
Nozaki
H.
(
1998
)
Purification of freshwater picoplanktonic cyanobacteria by pour-plating in ‘ultra-low-gelling-temperature agarose
.
Phycol. Res.
46
,
71
75
17.
Humbert
J.-F.
,
Barbe
V.
,
Latifi
A.
,
Gugger
M.
,
Calteau
A.
,
Coursin
T.
et al.
(
2013
)
A tribute to disorder in the genome of the bloom-forming freshwater cyanobacterium microcystis aeruginosa
.
PLoS ONE
8
,
e70747
[PubMed]
18.
Alvarenga
D.O.
,
Fiore
M.F.
and
Varani
A.M.
(
2017
)
A metagenomic approach to cyanobacterial genomics
.
Front. Microbiol.
8
,
809
,
[PubMed]
19.
Liu
Q.
,
Zhang
Y.
,
Wu
H.
,
Liu
F.
,
Peng
W.
,
Zhang
X.
et al.
(
2020
)
A review and perspective of EDNA application to eutrophication and HAB control in freshwater and marine ecosystems
.
Microorganisms
8
,
417
[PubMed]
20.
MacKeigan
P.W.
,
Garner
R.E.
,
Monchamp
M.-È.
,
Walsh
D.A.
,
Onana
V.E.
,
Kraemer
S.A.
et al.
(
2022
)
Comparing microscopy and DNA metabarcoding techniques for identifying cyanobacteria assemblages across hundreds of lakes
.
Harmful Algae
113
,
102187
[PubMed]
21.
Battchikova
N.
,
Muth-Pawlak
D.
and
Aro
E.-M.
(
2018
)
Proteomics of cyanobacteria: current horizons
.
Curr. Opin. Biotechnol.
54
,
65
71
[PubMed]
22.
Ow
S.Y.
and
Wright
P.C.
(
2009
)
Current trends in high throughput proteomics in cyanobacteria
.
FEBS Lett.
583
,
1744
1752
[PubMed]
23.
Pandhal
J.
,
Wright
P.C.
and
Biggs
C.A.
(
2008
)
Proteomics with a pinch of salt: a cyanobacterial perspective
.
Saline Syst.
4
,
1
[PubMed]
24.
Barrios-Llerena
M.E.
,
Chong
P.K.
,
Gan
C.S.
,
Snijders
A.P.L.
,
Reardon
K.F.
and
Wright
P.C.
(
2006
)
Shotgun proteomics of cyanobacteria—applications of experimental and data-mining techniques
.
Brief. Funct. Genomics
5
,
121
132
25.
Spät
P.
,
Maček
B.
and
Forchhammer
K.
(
2015
)
Phosphoproteome of the Cyanobacterium Synechocystis Sp. PCC 6803 and its dynamics during nitrogen starvation
.
Front. Microbiol.
6
,
[PubMed]
26.
Wang
J.
,
Huang
X.
,
Ge
H.
,
Wang
Y.
,
Chen
W.
,
Zheng
L.
et al.
(
2022
)
The Quantitative Proteome Atlas of a model cyanobacterium
.
J. Genet. Genomics
49
,
96
108
[PubMed]
27.
Zhang
Q.
,
Yu
S.
,
Wang
Q.
,
Yang
M.
and
Ge
F.
(
2021
)
Quantitative proteomics reveals the protein regulatory network of Anabaena Sp. PCC 7120 under nitrogen deficiency
.
J. Proteome Res.
20
,
3963
3976
[PubMed]
28.
Yang
M.
,
Yang
Y.
,
Chen
Z.
,
Zhang
J.
,
Lin
Y.
,
Wang
Y.
et al.
(
2014
)
Proteogenomic analysis and global discovery of posttranslational modifications in prokaryotes
.
Proc. Natl. Acad. Sci. U. S. A.
111
,
E5633
E5642
[PubMed]
29.
(
2021
)
The UniProt Consortium. UniProt: The Universal Protein Knowledgebase in 2021
.
Nucleic Acids Res.
49
,
D480
D489
[PubMed]
30.
Leney
A.C.
(
2019
)
Subunit PI can influence protein complex dissociation characteristics
.
J. Am. Soc. Mass. Spectrom.
30
,
1389
1395
[PubMed]
31.
Sonani
R.R.
,
Roszak
A.W.
,
Liu
H.
,
Gross
M.L.
,
Blankenship
R.E.
,
Madamwar
D.
et al.
(
2020
)
Revisiting high-resolution crystal structure of phormidium rubidum phycocyanin
.
Photosynth. Res.
144
,
349
360
[PubMed]
32.
de Souza
N.
and
Picotti
P.
(
2020
)
Mass spectrometry analysis of the structural proteome
.
Curr. Opin. Struct. Biol.
60
,
57
65
[PubMed]
33.
Lössl
P.
,
van de Waterbeemd
M.
and
Heck
A.J.
(
2016
)
The diverse and expanding role of mass spectrometry in structural and molecular biology
.
EMBO J.
35
,
2634
2657
[PubMed]
34.
Jumper
J.
,
Evans
R.
,
Pritzel
A.
,
Green
T.
,
Figurnov
M.
,
Ronneberger
O.
et al.
(
2021
)
Highly accurate protein structure prediction with AlphaFold
.
Nature
596
,
583
589
[PubMed]
35.
Assaiya
A.
,
Burada
A.P.
,
Dhingra
S.
and
Kumar
J.
(
2021
)
An overview of the recent advances in cryo-electron microscopy for life sciences
.
Emerg. Top. Life Sci.
5
,
151
168
[PubMed]
36.
Cheng
Y.
(
2018
)
Single-particle Cryo-EM-how did it get here and where will it go
.
Science
361
,
876
880
[PubMed]
37.
Britt
H.M.
,
Cragnolini
T.
and
Thalassinos
K.
(
2022
)
Integration of mass spectrometry data for structural biology
.
Chem. Rev.
122
,
7952
7986
[PubMed]
38.
Tamara
S.
,
den Boer
M.A.
and
Heck
A.J.R.
(
2022
)
High-resolution native mass spectrometry
.
Chem. Rev.
122
,
7269
7326
[PubMed]
39.
Brodbelt
J.S.
(
2022
)
Deciphering combinatorial post-translational modifications by top-down mass spectrometry
.
Curr. Opin. Chem. Biol.
70
,
102180
[PubMed]
40.
Vallejo
D.D.
,
Rojas Ramírez
C.
,
Parson
K.F.
,
Han
Y.
,
Gadkari
V.V.
and
Ruotolo
B.T.
(
2022
)
Mass spectrometry methods for measuring protein stability
.
Chem. Rev.
122
,
7690
7719
[PubMed]
41.
Tong
W.
and
Wang
G.
(
2018
)
How can native mass spectrometry contribute to characterization of biomacromolecular higher-order structure and interactions?
Methods
144
,
3
13
[PubMed]
42.
Ben-Nissan
G.
and
Sharon
M.
(
2018
)
The application of ion-mobility mass spectrometry for structure/function investigation of protein complexes
.
Curr. Opin. Chem. Biol.
42
,
25
33
[PubMed]
43.
Pukala
T.
(
2019
)
Importance of collision cross section measurements by ion mobility mass spectrometry in structural biology
.
Rapid Commun. Mass Spectrom.
33
,
72
82
[PubMed]
44.
Kalenius
E.
,
Groessl
M.
and
Rissanen
K.
(
2019
)
Ion mobility-mass spectrometry of supramolecular complexes and assemblies
.
Nat. Rev. Chem.
3
,
4
14
45.
Leney
A.C.
and
Heck
A.J.R.
(
2017
)
Native mass spectrometry: what is in the name?
J. Am. Soc. Mass. Spectrom.
28
,
5
13
46.
Trabjerg
E.
,
Nazari
Z.E.
and
Rand
K.D.
(
2018
)
Conformational analysis of complex protein states by hydrogen/deuterium exchange mass spectrometry (HDX-MS): challenges and emerging solutions
.
TrAC Trends Anal. Chem.
106
,
125
138
47.
James
E.I.
,
Murphree
T.A.
,
Vorauer
C.
,
Engen
J.R.
and
Guttman
M.
(
2022
)
Advances in hydrogen/deuterium exchange mass spectrometry and the pursuit of challenging biological systems
.
Chem. Rev.
122
,
7562
7623
[PubMed]
48.
Li
K.S.
,
Shi
L.
and
Gross
M.L.
(
2018
)
Mass spectrometry-based fast photochemical oxidation of proteins (FPOP) for higher order structure characterization
.
Acc. Chem. Res.
51
,
736
744
[PubMed]
49.
McKenzie-Coe
A.
,
Montes
N.S.
and
Jones
L.M.
(
2022
)
Hydroxyl radical protein footprinting: a mass spectrometry-based structural method for studying the higher order structure of proteins
.
Chem. Rev.
122
,
7532
7561
[PubMed]
50.
Liu
R.
,
Xia
S.
and
Li
H.
(
2022
)
Native top-down mass spectrometry for higher-order structural characterization of proteins and complexes
.
Mass Spectrom. Rev. (n/a)
e21793
51.
Petrotchenko
E.V.
and
Borchers
C.H.
(
2022
)
Protein chemistry combined with mass spectrometry for protein structure determination
.
Chem. Rev.
122
,
7488
7499
[PubMed]
52.
O'Reilly
F.J.
and
Rappsilber
J.
(
2018
)
Cross-linking mass spectrometry: methods and applications in structural, molecular and systems biology
.
Nat. Struct. Mol. Biol.
25
,
1000
1008
[PubMed]
53.
Yu
C.
and
Huang
L.
(
2018
)
Cross-linking mass spectrometry (XL-MS): an emerging technology for interactomics and structural biology
.
Anal. Chem.
90
,
144
165
[PubMed]
54.
Skinner
O.S.
,
Haverland
N.A.
,
Fornelli
L.
,
Melani
R.D.
,
Do Vale
L.H.F.
,
Seckler
H.S.
et al.
(
2018
)
Top-down characterization of endogenous protein complexes with native proteomics
.
Nat. Chem. Biol.
14
,
36
41
[PubMed]
55.
Rolland
A.D.
and
Prell
J.S.
(
2022
)
Approaches to heterogeneity in native mass spectrometry
.
Chem. Rev.
122
,
7909
7951
[PubMed]
56.
Garcia-Alles
L.F.
,
Lesniewska
E.
,
Root
K.
,
Aubry
N.
,
Pocholle
N.
,
Mendoza
C.I.
et al.
(
2017
)
Spontaneous non-canonical assembly of CcmK hexameric components from β-carboxysome shells of cyanobacteria
.
PloS ONE
12
,
e0185109
[PubMed]
57.
Guerreiro
A.C.L.
,
Penning
R.
,
Raaijmakers
L.M.
,
Axman
I.M.
,
Heck
A.J.R.
and
Altelaar
A.F.M.
(
2016
)
Monitoring light/dark association dynamics of multi-protein complexes in cyanobacteria using size exclusion chromatography-based proteomics
.
J. Proteomics
142
,
33
44
[PubMed]
58.
Bellamy-Carter
J.
,
Sound
J.K.
and
Leney
A.C.
(
2022
)
Probing heavy metal binding to phycobiliproteins
.
FEBS J.
289
,
4646
4656
[PubMed]
59.
Kaldmäe
M.
,
Sahin
C.
,
Saluri
M.
,
Marklund
E.G.
and
Landreh
M.
(
2019
)
A strategy for the identification of protein architectures directly from ion mobility mass spectrometry data reveals stabilizing subunit interactions in light harvesting complexes
.
Protein Sci. Publ. Protein Soc.
28
,
1024
1030
60.
Baniulis
D.
,
Yamashita
E.
,
Whitelegge
J.P.
,
Zatsman
A.I.
,
Hendrich
M.P.
,
Hasan
S.S.
et al.
(
2009
)
Structure-function, stability, and chemical modification of the cyanobacterial cytochrome B6f complex from Nostoc Sp. PCC 7120*
.
J. Biol. Chem.
284
,
9861
9869
[PubMed]
61.
Ryan
C.M.
,
Souda
P.
,
Bassilian
S.
,
Ujwal
R.
,
Zhang
J.
,
Abramson
J.
et al.
(
2010
)
Post-translational modifications of integral membrane proteins resolved by top-down fourier transform mass spectrometry with collisionally activated dissociation
.
Mol. Cell. Proteomics MCP
9
,
791
803
62.
Liu
H.
,
Zhang
H.
,
Niedzwiedzki
D.M.
,
Prado
M.
,
He
G.
,
Gross
M.L.
et al.
(
2013
)
Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria
.
Science
342
,
1104
1107
[PubMed]
63.
Gupta
S.
,
Sutter
M.
,
Remesh
S.G.
,
Dominguez-Martin
M.A.
,
Bao
H.
,
Feng
X.A.
et al.
(
2019
)
X-ray radiolytic labeling reveals the molecular basis of orange carotenoid protein photoprotection and its interactions with fluorescence recovery protein
.
J. Biol. Chem.
294
,
8848
8860
[PubMed]
64.
Mann
M.
and
Jensen
O.N.
(
2003
)
Proteomic analysis of post-translational modifications
.
Nat. Biotechnol.
21
,
255
261
[PubMed]
65.
Doll
S.
and
Burlingame
A.L.
(
2015
)
Mass spectrometry-based detection and assignment of protein posttranslational modifications
.
ACS Chem. Biol.
10
,
63
71
[PubMed]
66.
Virág
D.
,
Dalmadi-Kiss
B.
,
Vékey
K.
,
Drahos
L.
,
Klebovich
I.
,
Antal
I.
et al.
(
2020
)
Current trends in the analysis of post-translational modifications
.
Chromatographia
83
,
1
10
67.
Macek
B.
,
Forchhammer
K.
,
Hardouin
J.
,
Weber-Ban
E.
,
Grangeasse
C.
and
Mijakovic
I.
(
2019
)
Protein post-translational modifications in bacteria
.
Nat. Rev. Microbiol.
17
,
651
664
[PubMed]
68.
Glazer
A.N.
(
1994
)
Phycobiliproteins — a family of valuable, widely used fluorophores
.
J. Appl. Phycol.
6
,
105
112
69.
Vernon
T.
,
Glazer
A.N.
and
Stryer
L.
(
1982
)
Fluorescent phycobiliprotein conjugates for analyses of cells and molecules
.
J. Cell Biol.
93
,
981
986
[PubMed]
70.
Kronick
M.N.
(
1986
)
The use of phycobiliproteins as fluorescent labels in immunoassay
.
J. Immunol. Methods
92
,
1
13
[PubMed]
71.
Li
Y.
,
Zhang
Z.
,
Paciulli
M.
and
Abbaspourrad
A.
(
2020
)
Extraction of phycocyanin—a natural blue colorant from dried spirulina biomass: influence of processing parameters and extraction techniques
.
J. Food Sci.
85
,
727
735
[PubMed]
72.
Martelli
G.
,
Folli
C.
,
Visai
L.
,
Daglia
M.
and
Ferrari
D.
(
2014
)
Thermal stability improvement of blue colorant c-phycocyanin from spirulina platensis for food industry applications
.
Process Biochem.
49
,
154
159
73.
Jespersen
L.
,
Strømdahl
L.D.
,
Olsen
K.
and
Skibsted
L.H.
(
2005
)
Heat and light stability of three natural blue colorants for use in confectionery and beverages
.
Eur. Food Res. Technol.
220
,
261
266
74.
Hamed
I.
(
2016
)
The evolution and versatility of microalgal biotechnology: a review
.
Compr. Rev. Food Sci. Food Saf.
15
,
1104
1123
[PubMed]
75.
Begum
H.
,
Yusoff
F.M.D.
,
Banerjee
S.
,
Khatoon
H.
and
Shariff
M.
(
2016
)
Availability and utilization of pigments from microalgae
.
Crit. Rev. Food Sci. Nutr.
56
,
2209
2222
[PubMed]
76.
Gallon
J.R.
,
Cheng
J.
,
Dougherty
L.J.
,
Gallon
V.A.
,
Hilz
H.
,
Pederson
D.M.
et al.
(
2000
)
A novel covalent modification of nitrogenase in a cyanobacterium
.
FEBS Lett.
468
,
231
233
[PubMed]
77.
Ekman
M.
,
Tollbäck
P.
and
Bergman
B.
(
2008
)
Proteomic analysis of the cyanobacterium of the azolla symbiosis: identity, adaptation, and NifH modification
.
J. Exp. Bot.
59
,
1023
1034
[PubMed]
78.
Miller
C.A.
,
Leonard
H.S.
,
Pinsky
I.G.
,
Turner
B.M.
,
Williams
S.R.
,
Harrison
L.
et al.
(
2008
)
Biogenesis of Phycobiliproteins: III. CpcM is the asparagine methyltransferase for phycobiliprotein β-subunits in cyanobacteria*
.
J. Biol. Chem.
283
,
19293
19300
[PubMed]
79.
Schluchter
W.M.
,
Shen
G.
,
Alvey
R.M.
,
Biswas
A.
,
Saunée
N.A.
,
Williams
S.R.
et al.
(
2010
)
Phycobiliprotein biosynthesis in cyanobacteria: structure and function of enzymes involved in post-translational modification
. In
Recent Advances in Phototrophic Prokaryotes
(
Hallenbeck
P.C.
, ed.), pp.
211
228
,
Springer
,
New York, NY
,
Ed.; (Advances in Experimental Medicine and Biology)
80.
Bryant
D.A.
,
Cohen-Bazire
G.
and
Glazer
A.N.
(
1981
)
Characterization of the biliproteins of gloeobacter violaceus chromophore content of a cyanobacterial phycoerythrin carrying phycourobilin chromophore
.
Arch. Microbiol.
129
,
190
198
81.
Ong
L.J.
and
Glazer
A.N.
(
1991
)
Phycoerythrins of Marine Unicellular Cyanobacteria. I. Bilin Types and Locations and Energy Transfer Pathways in Synechococcus Spp. Phycoerythrins
.
J. Biol. Chem.
266
,
9515
9527
[PubMed]
82.
Klotz
A.V.
,
Leary
J.A.
and
Glazer
A.N.
(
1986
)
Post-translational methylation of asparaginyl residues. Identification of beta-71 gamma-N-methylasparagine in allophycocyanin
.
J. Biol. Chem.
261
,
15891
15894
[PubMed]
83.
Klotz
A.V.
and
Glazer
A.N.
(
1987
)
Gamma-N-methylasparagine in phycobiliproteins. Occurrence, location, and biosynthesis
.
J. Biol. Chem.
262
,
17350
17355
[PubMed]
84.
Piven
I.
,
Ajlani
G.
and
Sokolenko
A.
(
2005
)
Phycobilisome linker proteins are phosphorylated in Synechocystis Sp. PCC 6803*
.
J. Biol. Chem.
280
,
21667
21672
[PubMed]
85.
Hongsthong
A.
,
Sirijuntarut
M.
,
Prommeenate
P.
,
Lertladaluck
K.
,
Porkaew
K.
,
Cheevadhanarak
S.
et al.
(
2008
)
Proteome analysis at the subcellular level of the cyanobacterium spirulina platensis in response to low-temperature stress conditions
.
FEMS Microbiol. Lett.
288
,
92
101
[PubMed]
86.
Hongsthong
A.
,
Sirijuntarut
M.
,
Yutthanasirikul
R.
,
Senachak
J.
,
Kurdrid
P.
,
Cheevadhanarak
S.
et al.
(
2009
)
Subcellular proteomic characterization of the high-temperature stress response of the cyanobacterium spirulina platensis
.
Proteome Sci.
7
,
33
[PubMed]
87.
Kehoe
D.M.
and
Grossman
A.R.
(
1997
)
New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system
.
J. Bacteriol.
179
,
3914
3921
[PubMed]
88.
Sobczyk
A.
,
Schyns
G.
,
Tandeau de Marsac
N.
and
Houmard
J.
(
1993
)
Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix Sp. PCC 7601: DNA-binding proteins and modulation by phosphorylation
.
EMBO J.
12
,
997
1004
[PubMed]
89.
Sobczyk
A.
,
Bely
A.
,
de Marsac
N.T.
and
Houmard
J.
(
1994
)
A phosphorylated DNA-binding protein is specific for the red-light signal during complementary chromatic adaptation in cyanobacteria
.
Mol. Microbiol.
13
,
875
885
[PubMed]
90.
Tsinoremas
N.F.
,
Castets
A.M.
,
Harrison
M.A.
,
Allen
J.F.
and
De Marsac
N.T.
(
1991
)
Photosynthetic electron transport controls nitrogen assimilation in cyanobacteria by means of posttranslational modification of the GlnB gene product
.
Proc. Natl. Acad. Sci. U.S.A.
88
,
4565
4569
[PubMed]
91.
Forchhammer
K.
and
Tandeau de Marsac
N.
(
1994
)
The PII Protein in the Cyanobacterium Synechococcus Sp. Strain PCC 7942 is modified by serine phosphorylation and signals the cellular N-status
.
J. Bacteriol.
176
,
84
91
[PubMed]
92.
Forchhammer
K.
and
Tandeau de Marsac
N.
(
1995
)
Phosphorylation of the PII Protein (GlnB Gene Product) in the Cyanobacterium Synechococcus Sp. Strain PCC 7942: Analysis of in Vitro Kinase Activity
.
J. Bacteriol.
177
,
5812
5817
[PubMed]
93.
Forchhammer
K.
(
2004
)
Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets
.
FEMS Microbiol. Rev.
28
,
319
333
[PubMed]
94.
Forchhammer
K.
and
Tandeau de Marsac
N.
(
1995
)
Functional analysis of the phosphoprotein PII (GlnB Gene Product) in the Cyanobacterium Synechococcus Sp. Strain PCC 7942
.
J. Bacteriol.
177
,
2033
2040
[PubMed]
95.
Nishiwaki
T.
,
Iwasaki
H.
,
Ishiura
M.
and
Kondo
T.
(
2000
)
Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria
.
Proc. Natl. Acad. Sci.
97
,
495
499
96.
Iwasaki
H.
,
Nishiwaki
T.
,
Kitayama
Y.
,
Nakajima
M.
and
Kondo
T.
(
2002
)
KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria
.
Proc. Natl. Acad. Sci.
99
,
15788
15793
97.
Xu
Y.
,
Mori
T.
and
Johnson
C.H.
(
2003
)
Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the KaiBC promoter in regulating KaiC
.
EMBO J.
22
,
2117
2126
[PubMed]
98.
Kitayama
Y.
,
Iwasaki
H.
,
Nishiwaki
T.
and
Kondo
T.
(
2003
)
KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system
.
EMBO J.
22
,
2127
2134
[PubMed]
99.
Iwasaki
H.
,
Williams
S.B.
,
Kitayama
Y.
,
Ishiura
M.
,
Golden
S.S.
and
Kondo
T.
(
2000
)
A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria
.
Cell
101
,
223
233
[PubMed]
100.
Yu
S.
,
Yang
M.
,
Xiong
J.
,
Zhang
Q.
,
Gao
X.
,
Miao
W.
et al.
(
2021
)
Proteogenomic analysis provides novel insight into genome annotation and nitrogen metabolism in Nostoc Sp. PCC 7120
.
Microbiol. Spectr.
9
,
e00490
e00521
[PubMed]
101.
Mikkat
S.
,
Fulda
S.
and
Hagemann
M.
(
2014
)
A 2D gel electrophoresis-based snapshot of the phosphoproteome in the cyanobacterium synechocystis Sp. Strain PCC 6803
.
Microbiology
160
,
296
306
[PubMed]
102.
Lee
D.-G.
,
Kwon
J.
,
Eom
C.-Y.
,
Kang
Y.-M.
,
Roh
S.W.
,
Lee
K.-B.
et al.
(
2015
)
Directed analysis of cyanobacterial membrane phosphoproteome using stained phosphoproteins and titanium-enriched phosphopeptides
.
J. Microbiol.
53
,
279
287
[PubMed]
103.
Chen
Z.
,
Zhan
J.
,
Chen
Y.
,
Yang
M.
,
He
C.
,
Ge
F.
et al.
(
2015
)
Effects of phosphorylation of β subunits of phycocyanins on state transition in the model Cyanobacterium Synechocystis Sp. PCC 6803
.
Plant Cell Physiol.
56
,
1997
2013
[PubMed]
104.
Zorina
A.
,
Stepanchenko
N.
,
Novikova
G.V.
,
Sinetova
M.
,
Panichkin
V.B.
,
Moshkov
I.E.
et al.
(
2011
)
Eukaryotic-like Ser/Thr protein kinases SpkC/F/K Are involved in phosphorylation of GroES in the Cyanobacterium Synechocystis
.
DNA Res.
18
,
137
151
[PubMed]
105.
Yang
M.
,
Qiao
Z.
,
Zhang
W.
,
Xiong
Q.
,
Zhang
J.
,
Li
T.
et al.
(
2013
)
Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model Cyanobacterium Synechococcus Sp. Strain PCC 7002
.
J. Proteome Res.
12
,
1909
1923
[PubMed]
106.
Angeleri
M.
,
Zorina
A.
,
Aro
E.-M.
and
Battchikova
N.
(
2018
)
Interplay of SpkG Kinase and the Slr0151 Protein in the Phosphorylation of Ferredoxin 5 in Synechocystis Sp. Strain PCC 6803
.
FEBS Lett.
592
,
411
421
[PubMed]
107.
Angeleri
M.
,
Muth-Pawlak
D.
,
Aro
E.-M.
and
Battchikova
N.
(
2016
)
Study of O-phosphorylation sites in proteins involved in photosynthesis-related processes in Synechocystis Sp. Strain PCC 6803: application of the SRM approach
.
J. Proteome Res.
15
,
4638
4652
[PubMed]
108.
Mo
R.
,
Yang
M.
,
Chen
Z.
,
Cheng
Z.
,
Yi
X.
,
Li
C.
et al.
(
2015
)
Acetylome analysis reveals the involvement of lysine acetylation in photosynthesis and carbon metabolism in the model Cyanobacterium Synechocystis Sp. PCC 6803
.
J. Proteome Res.
14
,
1275
1286
[PubMed]
109.
Chen
Z.
,
Zhang
G.
,
Yang
M.
,
Li
T.
,
Ge
F.
and
Zhao
J.
(
2017
)
Lysine acetylome analysis reveals photosystem II manganese-stabilizing protein acetylation is involved in negative regulation of oxygen evolution in model Cyanobacterium Synechococcus Sp. PCC 7002
.
Mol. Cell. Proteomics
16
,
1297
1311
[PubMed]
110.
Chardonnet
S.
,
Sakr
S.
,
Cassier-Chauvat
C.
,
Le Maréchal
P.
,
Chauvat
F.
,
Lemaire
S.D.
et al.
(
2015
)
First proteomic study of S-glutathionylation in cyanobacteria
.
J. Proteome Res.
14
,
59
71
[PubMed]
111.
Lambertz
J.
,
Liauw
P.
,
Whitelegge
J.P.
and
Nowaczyk
M.M.
(
2021
)
Mass spectrometry analysis of the photosystem II assembly factor Psb27 revealed variations in its lipid modification
.
Photosynth. Res.
152
,
305
316
[PubMed]
112.
Nowaczyk
M.M.
,
Hebeler
R.
,
Schlodder
E.
,
Meyer
H.E.
,
Warscheid
B.
and
Rögner
M.
(
2006
)
Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II
.
Plant Cell
18
,
3121
3131
[PubMed]
113.
Yang
M.
,
Huang
H.
and
Ge
F.
(
2019
)
Lysine propionylation is a widespread post-translational modification involved in regulation of photosynthesis and metabolism in cyanobacteria
.
Int. J. Mol. Sci.
20
,
4792
[PubMed]
114.
Liu
X.
,
Yang
M.
,
Liu
Y.
,
Ge
F.
and
Zhao
J.
(
2020
)
Structural and functional insights into a lysine deacylase in the Cyanobacterium Synechococcus Sp. PCC 7002
.
Plant Physiol.
184
,
762
776
[PubMed]
115.
Ma
Y.
,
Yang
M.
,
Lin
X.
,
Liu
X.
,
Huang
H.
and
Ge
F.
(
2017
)
Malonylome analysis reveals the involvement of lysine malonylation in metabolism and photosynthesis in cyanobacteria
.
J. Proteome Res.
16
,
2030
2043
[PubMed]
116.
Liu
X.
,
Yang
M.
,
Wang
Y.
,
Chen
Z.
,
Zhang
J.
,
Lin
X.
et al.
(
2018
)
Effects of PSII manganese-stabilizing protein succinylation on photosynthesis in the model Cyanobacterium Synechococcus Sp. PCC 7002
.
Plant Cell Physiol.
59
,
1466
1482
[PubMed]
117.
Li
X.
,
Wang
L.
,
Wang
M.
,
Zhang
Z.
,
Ma
C.
,
Ma
X.
et al.
(
2021
)
Global analysis of protein succinylation modification of nostoc flagelliforme in response to dehydration
.
J. Proteomics
237
,
104149
[PubMed]
118.
Zilliges
Y.
,
Kehr
J.-C.
,
Mikkat
S.
,
Bouchier
C.
,
de Marsac
N.T.
,
Börner
T.
et al.
(
2008
)
An extracellular glycoprotein is implicated in cell-cell contacts in the toxic Cyanobacterium Microcystis Aeruginosa PCC 7806
.
J. Bacteriol.
190
,
2871
2879
[PubMed]
119.
Li
B.
,
Jo
M.
,
Liu
J.
,
Tian
J.
,
Canfield
R.
and
Bridwell-Rabb
J.
(
2022
)
Structural and mechanistic basis for redox sensing by the cyanobacterial transcription regulator RexT
.
Commun. Biol.
5
,
1
15
[PubMed]
120.
Nishiwaki
T.
,
Satomi
Y.
,
Kitayama
Y.
,
Terauchi
K.
,
Kiyohara
R.
,
Takao
T.
et al.
(
2007
)
A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria
.
EMBO J.
26
,
4029
4037
[PubMed]
121.
Rust
M.J.
,
Markson
J.S.
,
Lane
W.S.
,
Fisher
D.S.
and
O'Shea
E.K.
(
2007
)
Ordered phosphorylation governs oscillation of a three-protein circadian clock
.
Science
318
,
809
812
[PubMed]
122.
Gutu
A.
and
O'Shea
E.K.
(
2013
)
Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression
.
Mol. Cell
50
,
288
294
[PubMed]
123.
Markson
J.S.
,
Piechura
J.R.
,
Puszynska
A.M.
and
O'Shea
E.K.
(
2013
)
Circadian control of global gene expression by the cyanobacterial master regulator RpaA
.
Cell
155
,
1396
1408
[PubMed]
124.
McIntosh
J.A.
,
Donia
M.S.
,
Nair
S.K.
and
Schmidt
E.W.
(
2011
)
Enzymatic basis of ribosomal peptide prenylation in cyanobacteria
.
J. Am. Chem. Soc.
133
,
13698
13705
[PubMed]
125.
Martins
J.
,
Leikoski
N.
,
Wahlsten
M.
,
Azevedo
J.
,
Antunes
J.
,
Jokela
J.
et al.
(
2018
)
Sphaerocyclamide, a prenylated cyanobactin from the Cyanobacterium Sphaerospermopsis Sp. LEGE 00249
.
Sci. Rep.
8
,
14537
[PubMed]
126.
Phyo
M.Y.
,
Ding
C.Y.G.
,
Goh
H.C.
,
Goh
J.X.
,
Ong
J.F.M.
,
Chan
S.H.
et al.
(
2019
)
Trikoramide A, a prenylated cyanobactin from the marine cyanobacterium symploca hydnoides
.
J. Nat. Prod.
82
,
3482
3488
[PubMed]
127.
Morita
M.
,
Hao
Y.
,
Jokela
J.K.
,
Sardar
D.
,
Lin
Z.
,
Sivonen
K.
et al.
(
2018
)
Posttranslational tyrosine geranylation in cyanobactin biosynthesis
.
J. Am. Chem. Soc.
140
,
6044
6048
[PubMed]
128.
Martins
J.
and
Vasconcelos
V.
(
2015
)
Cyanobactins from cyanobacteria: current genetic and chemical state of knowledge
.
Mar. Drugs
13
,
6910
6946
[PubMed]
129.
Gu
W.
,
Dong
S.-H.
,
Sarkar
S.
,
Nair
S.K.
and
Schmidt
E.W.
(
2018
)
The biochemistry and structural biology of cyanobactin biosynthetic enzymes
.
Methods Enzymol.
604
,
113
163
[PubMed]
130.
Kim
M.-S.
,
Zhong
J.
and
Pandey
A.
(
2016
)
Common errors in mass spectrometry-based analysis of post-translational modifications
.
Proteomics
16
,
700
714
[PubMed]
131.
Snijder
J.
,
Schuller
J.M.
,
Wiegard
A.
,
Lössl
P.
,
Schmelling
N.
,
Axmann
I.M.
et al.
(
2017
)
Structures of the cyanobacterial circadian oscillator frozen in a fully assembled state
.
Science
355
,
1181
1184
[PubMed]
132.
Sound
J.K.
,
Peters
A.
,
Bellamy-Carter
J.
,
Rad-Menéndez
C.
,
MacKechnie
K.
,
Green
D.H.
et al.
(
2021
)
Rapid cyanobacteria species identification with high sensitivity using native mass spectrometry
.
Anal. Chem.
93
,
14293
14299
[PubMed]
133.
Knoppová
J.
,
Yu
J.
,
Janouškovec
J.
,
Halada
P.
,
Nixon
P.J.
,
Whitelegge
J.P.
et al.
(
2021
)
The Photosystem II Assembly Factor Ycf48 from the Cyanobacterium Synechocystis Sp. PCC 6803 is lipidated using an atypical lipobox sequence
.
Int. J. Mol. Sci.
22
,
3733
[PubMed]
134.
Nagarajan
A.
,
Zhou
M.
,
Nguyen
A.Y.
,
Liberton
M.
,
Kedia
K.
,
Shi
T.
et al.
(
2019
)
Proteomic insights into phycobilisome degradation, a selective and tightly controlled process in the fast-growing Cyanobacterium Synechococcus Elongatus UTEX 2973
.
Biomolecules
9
,
374
[PubMed]
135.
Lin
X.
,
Yang
M.
,
Liu
X.
,
Cheng
Z.
and
Ge
F.
(
2020
)
Characterization of lysine monomethylome and methyltransferase in model Cyanobacterium Synechocystis Sp. PCC 6803
.
Genomics Proteomics Bioinformatics
18
,
289
304
[PubMed]
136.
Nishiwaki
T.
,
Satomi
Y.
,
Nakajima
M.
,
Lee
C.
,
Kiyohara
R.
,
Kageyama
H.
et al.
(
2004
)
Role of KaiC phosphorylation in the circadian clock system of Synechococcus Elongatus PCC 7942
.
Proc. Natl. Acad. Sci.
101
,
13927
13932
137.
El-Fahmawi
B.
and
Owttrim
G.W.
(
2007
)
Cold-stress-altered phosphorylation of EF-Tu in the Cyanobacterium Anabaena Sp. Strain PCC 7120
.
Can. J. Microbiol.
53
,
551
558
[PubMed]
138.
Spät
P.
,
Klotz
A.
,
Rexroth
S.
,
Maček
B.
and
Forchhammer
K.
(
2018
)
Chlorosis as a developmental program in cyanobacteria: the proteomic fundament for survival and awakening *
.
Mol. Cell. Proteomics
17
,
1650
1669
[PubMed]
139.
Kronfel
C.M.
,
Hernandez
C.V.
,
Frick
J.P.
,
Hernandez
L.S.
,
Gutu
A.
,
Karty
J.A.
et al.
(
2019
)
CpeF is the bilin lyase that ligates the doubly linked phycoerythrobilin on β-Phycoerythrin in the cyanobacterium fremyella diplosiphon
.
J. Biol. Chem.
294
,
3987
3999
[PubMed]
140.
Nixon
P.J.
,
Trost
J.T.
and
Diner
B.A.
(
1992
)
Role of the carboxy-terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the Cyanobacterium synechocystis Sp. PCC 6803:assembly requires a free carboxyl group at C-terminal position 344
.
Biochemistry
31
,
10859
10871
[PubMed]
141.
Guerreiro
A.C.L.
,
Benevento
M.
,
Lehmann
R.
,
van Breukelen
B.
,
Post
H.
,
Giansanti
P.
et al.
(
2014
)
Daily rhythms in the cyanobacterium synechococcus elongatus probed by high-resolution mass spectrometry-based proteomics reveals a small defined set of cyclic proteins
.
Mol. Cell. Proteomics MCP
13
,
2042
2055
142.
Bryan
S.J.
,
Burroughs
N.J.
,
Shevela
D.
,
Yu
J.
,
Rupprecht
E.
,
Liu
L.-N.
et al.
(
2014
)
Localisation and interactions of the Vipp1 protein in cyanobacteria
.
Mol. Microbiol.
94
,
1179
1195
[PubMed]
143.
Xu
C.
,
Wang
B.
,
Yang
L.
,
Zhongming Hu
L.
,
Yi
L.
,
Wang
Y.
et al.
(
2021
)
Global landscape of native protein complexes in synechocystis Sp. PCC 6803
.
Genomics Proteomics Bioinformatics
S1672
0229(21)00037-1
[PubMed]
144.
Ladig
R.
,
Sommer
M.S.
,
Hahn
A.
,
Leisegang
M.S.
,
Papasotiriou
D.G.
,
Ibrahim
M.
et al.
(
2011
)
A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes
.
Plant J. Cell Mol. Biol.
67
,
181
194
145.
Hackenberg
C.
,
Hakanpää
J.
,
Cai
F.
,
Antonyuk
S.
,
Eigner
C.
,
Meissner
S.
et al.
(
2018
)
Structural and functional insights into the unique CBS-CP12 fusion protein family in cyanobacteria
.
Proc. Natl. Acad. Sci.
115
,
7141
7146
146.
Eisenberg
I.
,
Harris
D.
,
Levi-Kalisman
Y.
,
Yochelis
S.
,
Shemesh
A.
,
Ben-Nissan
G.
et al.
(
2017
)
Concentration-based self-assembly of phycocyanin
.
Photosynth. Res.
134
,
39
49
[PubMed]
147.
Mikhailov
V.A.
,
Ståhlberg
F.
,
Clarke
A.K.
and
Robinson
C.V.
(
2015
)
Dual stoichiometry and subunit organization in the ClpP1/P2 protease from the Cyanobacterium Synechococcus Elongatus
.
J. Struct. Biol.
192
,
519
527
[PubMed]
148.
Andersson
F.I.
,
Tryggvesson
A.
,
Sharon
M.
,
Diemand
A.V.
,
Classen
M.
,
Best
C.
et al.
(
2009
)
Structure and function of a novel type of ATP-dependent Clp protease
.
J. Biol. Chem.
284
,
13519
13532
[PubMed]
149.
Kerfeld
C.A.
and
Melnicki
M.R.
(
2016
)
Assembly, function and evolution of cyanobacterial carboxysomes
.
Curr. Opin. Plant Biol.
31
,
66
75
[PubMed]
150.
Garcia-Alles
L.F.
,
Lesniewska
E.
,
Root
K.
,
Aubry
N.
,
Pocholle
N.
,
Mendoza
C.I.
et al.
(
2017
)
Spontaneous non-canonical assembly of CcmK hexameric components from β-carboxysome shells of cyanobacteria
.
PLoS ONE
12
,
e0185109
[PubMed]
151.
Garcia-Alles
L.F.
,
Root
K.
,
Maveyraud
L.
,
Aubry
N.
,
Lesniewska
E.
,
Mourey
L.
et al.
(
2019
)
Occurrence and stability of hetero-hexamer associations formed by β-carboxysome CcmK shell components
.
PLoS ONE
14
,
e0223877
[PubMed]
152.
Ryan
P.
,
Forrester
T.J.B.
,
Wroblewski
C.
,
Kenney
T.M.G.
,
Kitova
E.N.
,
Klassen
J.S.
et al.
(
2019
)
The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit
.
J. Biol. Chem.
294
,
2593
5195
[PubMed]
153.
Bhat
J.Y.
,
Miličić
G.
,
Thieulin-Pardo
G.
,
Bracher
A.
,
Maxwell
A.
,
Ciniawsky
S.
et al.
(
2017
)
Mechanism of enzyme repair by the AAA+ chaperone rubisco activase
.
Mol. Cell
67
,
744.e6
756.e6
[PubMed]
154.
Snijder
J.
,
Burnley
R.J.
,
Wiegard
A.
,
Melquiond
A.S.J.
,
Bonvin
A.M.J.J.
,
Axmann
I.M.
et al.
(
2014
)
Insight into cyanobacterial circadian timing from structural details of the KaiB-KaiC interaction
.
Proc. Natl. Acad. Sci. U.S.A.
111
,
1379
1384
[PubMed]
155.
Snijder
J.
,
Schuller
J.M.
,
Wiegard
A.
,
Lössl
P.
,
Schmelling
N.
,
Axmann
I.M.
et al.
(
2017
)
Structures of the cyanobacterial circadian oscillator frozen in a fully assembled state
.
Science
355
,
1181
1184
[PubMed]
156.
Yunoki
Y.
,
Ishii
K.
,
Yagi-Utsumi
M.
,
Murakami
R.
,
Uchiyama
S.
,
Yagi
H.
et al.
ATP hydrolysis by KaiC promotes its KaiA binding in the cyanobacterial circadian clock system
.
Life Sci. Alliance
2
,
e201900368
[PubMed]
157.
Zhang
H.
,
Cui
W.
,
Gross
M.L.
and
Blankenship
R.E.
(
2013
)
Native mass spectrometry of photosynthetic pigment-protein complexes
.
FEBS Lett.
587
,
1012
1020
[PubMed]
158.
Tal
O.
,
Trabelcy
B.
,
Gerchman
Y.
and
Adir
N.
(
2014
)
Investigation of phycobilisome subunit interaction interfaces by coupled cross-linking and mass spectrometry
.
J. Biol. Chem.
289
,
33084
33097
[PubMed]
159.
Liu
H.
,
Zhang
M.M.
,
Weisz
D.A.
,
Cheng
M.
,
Pakrasi
H.B.
and
Blankenship
R.E.
(
2021
)
Structure of cyanobacterial phycobilisome core revealed by structural modeling and chemical cross-linking
.
Sci. Adv.
7
,
eaba5743
[PubMed]
160.
Liu
H.
,
Weisz
D.A.
,
Zhang
M.M.
,
Cheng
M.
,
Zhang
B.
,
Zhang
H.
et al.
(
2019
)
Phycobilisomes Harbor FNRL in cyanobacteria
.
mBio
10
,
e00669
e00719
[PubMed]
161.
Nguyen
A.Y.
,
Bricker
W.P.
,
Zhang
H.
,
Weisz
D.A.
,
Gross
M.L.
and
Pakrasi
H.B.
(
2017
)
The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: implications for the mechanism of phycobilisome degradation
.
Photosynth. Res.
132
,
95
106
[PubMed]
162.
Domínguez-Martín
M.A.
,
Sauer
P.V.
,
Kirst
H.
,
Sutter
M.
,
Bína
D.
,
Greber
B.J.
et al.
(
2022
)
Structures of a phycobilisome in light-harvesting and photoprotected states
.
Nature
1
11
163.
Kawakami
K.
,
Hamaguchi
T.
,
Hirose
Y.
,
Kosumi
D.
,
Miyata
M.
,
Kamiya
N.
et al.
(
2022
)
Core and rod structures of a thermophilic cyanobacterial light-harvesting phycobilisome
.
Nat. Commun.
13
,
3389
[PubMed]
164.
Kirilovsky
D.
and
Kerfeld
C.A.
(
2016
)
Cyanobacterial photoprotection by the orange carotenoid protein
.
Nat. Plants
2
,
16180
[PubMed]
165.
Wilson
A.
,
Punginelli
C.
,
Gall
A.
,
Bonetti
C.
,
Alexandre
M.
,
Routaboul
J.-M.
et al.
(
2008
)
A photoactive carotenoid protein acting as light intensity sensor
.
Proc. Natl. Acad. Sci. U.S.A.
105
,
12075
12080
[PubMed]
166.
Kerfeld
C.A.
,
Melnicki
M.R.
,
Sutter
M.
and
Dominguez-Martin
M.A.
(
2017
)
Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs
.
New Phytol.
215
,
937
951
[PubMed]
167.
Lu
Y.
,
Liu
H.
,
Saer
R.G.
,
Zhang
H.
,
Meyer
C.M.
,
Li
V.L.
et al.
(
2017
)
Native mass spectrometry analysis of oligomerization states of fluorescence recovery protein and orange carotenoid protein: two proteins involved in the cyanobacterial photoprotection cycle
.
Biochemistry
56
,
160
166
[PubMed]
168.
Liu
H.
,
Zhang
H.
,
King
J.D.
,
Wolf
N.R.
,
Prado
M.
,
Gross
M.L.
et al.
(
2014
)
Mass spectrometry footprinting reveals the structural rearrangements of cyanobacterial orange carotenoid protein upon light activation
.
Biochim. Biophys. Acta
1837
,
1955
1963
[PubMed]
169.
Gupta
S.
,
Guttman
M.
,
Leverenz
R.L.
,
Zhumadilova
K.
,
Pawlowski
E.G.
,
Petzold
C.J.
et al.
(
2015
)
Local and global structural drivers for the photoactivation of the orange carotenoid protein
.
Proc. Natl. Acad. Sci.
112
,
E5567
E5574
170.
Leverenz
R.L.
,
Sutter
M.
,
Wilson
A.
,
Gupta
S.
,
Thurotte
A.
,
Bourcier de Carbon
C.
et al.
(
2015
)
A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection
.
Science
348
,
1463
1466
[PubMed]
171.
Zhang
H.
,
Liu
H.
,
Blankenship
R.E.
and
Gross
M.L.
(
2016
)
Isotope-encoded carboxyl group footprinting for mass spectrometry-based protein conformational studies
.
J. Am. Soc. Mass. Spectrom.
27
,
178
181
[PubMed]
172.
Zhang
H.
,
Liu
H.
,
Niedzwiedzki
D.M.
,
Prado
M.
,
Jiang
J.
,
Gross
M.L.
et al.
(
2014
)
Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein
.
Biochemistry
53
,
13
19
[PubMed]
173.
Harris
D.
,
Tal
O.
,
Jallet
D.
,
Wilson
A.
,
Kirilovsky
D.
and
Adir
N.
(
2016
)
Orange carotenoid protein burrows into the phycobilisome to provide photoprotection
.
Proc. Natl. Acad. Sci.
113
,
E1655
E1662
[PubMed]
174.
Lu
Y.
,
Liu
H.
,
Saer
R.
,
Li
V.L.
,
Zhang
H.
,
Shi
L.
et al.
(
2017
)
A molecular mechanism for nonphotochemical quenching in cyanobacteria
.
Biochemistry
56
,
2812
2823
[PubMed]
175.
Bečková
M.
,
Gardian
Z.
,
Yu
J.
,
Konik
P.
,
Nixon
P.J.
and
Komenda
J.
(
2017
)
Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis Sp. PCC 6803 to High Light
.
Mol. Plant
10
,
62
72
[PubMed]
176.
Liu
H.
,
Chen
J.
,
Huang
R.Y.-C.
,
Weisz
D.
,
Gross
M.L.
and
Pakrasi
H.B.
(
2013
)
Mass spectrometry-based footprinting reveals structural dynamics of loop E of the chlorophyll-binding protein CP43 during photosystem II assembly in the Cyanobacterium Synechocystis 6803*
.
J. Biol. Chem.
288
,
14212
14220
[PubMed]
177.
Liu
H.
,
Huang
R.Y.-C.
,
Chen
J.
,
Gross
M.L.
and
Pakrasi
H.B.
(
2011
)
Psb27, a transiently associated protein, binds to the chlorophyll binding protein CP43 in photosystem II assembly intermediates
.
Proc. Natl. Acad. Sci.
108
,
18536
18541
178.
Cormann
K.U.
,
Möller
M.
and
Nowaczyk
M.M.
(
2016
)
Critical assessment of protein cross-linking and molecular docking: an updated model for the interaction between photosystem II and Psb27
.
Front. Plant Sci.
7
,
1
14
[PubMed]
179.
Boehm
M.
,
Yu
J.
,
Reisinger
V.
,
Beckova
M.
,
Eichacker
L.A.
,
Schlodder
E.
et al.
(
2012
)
Subunit composition of CP43-less photosystem II complexes of synechocystis Sp. PCC 6803: implications for the assembly and repair of photosystem II
.
Philos. Trans. R. Soc. B Biol. Sci.
367
,
3444
3454
180.
Weisz
D.A.
,
Liu
H.
,
Zhang
H.
,
Thangapandian
S.
,
Tajkhorshid
E.
,
Gross
M.L.
et al.
(
2017
)
Mass Spectrometry-based cross-linking study shows that the Psb28 protein binds to cytochrome B559 in photosystem II
.
Proc. Natl. Acad. Sci. U.S.A.
114
,
2224
2229
[PubMed]
181.
Liu
H.
(
2022
)
AlphaFold and structural mass spectrometry enable interrogations on the intrinsically disordered regions in cyanobacterial light-harvesting complex phycobilisome
.
J. Mol. Biol.
434
,
167831
[PubMed]
This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution License 4.0 (CC BY).