Current Trends of Bacterial and Fungal Optoproteins for Novel Optical Applications
Abstract
:1. Introduction
2. Photoreceptors Classification
- Light-oxygen-voltage (LOV) proteins form a group of photoreceptors that bind different flavins such as flavin mononucleotide (FMN) or flavin adenine dinucleotide (FAD) and respond to blue illumination (400–473 nm) eliciting several physiological responses across archaea, bacteria, protists, fungi, and plants. LOV receptors also serve as genetically encoded actuators in optogenetics for the spatiotemporally precise control of protein expression, cellular state, and processes [19]. The light responses of LOV are enhanced due to photochemical and structural mechanisms; they have been characterized in detail in [20,21]. LOV domains form internal protein-flavin adducts that generate conformational changes that control effector function [22]. In bacteria, LOV proteins are intrinsically related to a range of signal transduction output domains, such as histidine kinases, diguanylate cyclase-phosphodiesterases, and DNA-binding domains [23].
- Plant phytochromes (Phys) constitute a large receptor family sensitive to red and far-red light that occur in plants and employ as chromophores linear tetrapyrroles (bilins). These proteins have a photointerconvertible switch between two forms throughout the photoisomerization of the chromophores. These two forms can absorb red or far-red light and are designated as Pr and Pfr, respectively. They act as proximity sensors to modify plant growth and development [24]. Phytochromes are structurally classified according to the number of domains in their photosensory core module (PCM). Members of the “canonical” phytochrome subfamily (from bacteria, cyanobacteria, and plants) contain three domains in their PCM (PAS, Per-ARNT-Sim; GAF, cGMP phosphodiesterase-adenylate cyclase-FhlA; PHY, phytochrome-specific domain) and an output effector module, which is typically represented by histidine kinase (HisK). Despite the amino acid sequences of these domains showing low sequence similarity, their structures share a common topology.
- Algal phytochromes cover the entire visible and near-infrared spectrum. Compared to land plants, algae have a different type of phytochrome, since red and far-red light do not penetrate water to depths greater than a few meters. This kind of protein exhibits a great diversity of photocycles (yellow/ far-red, orange/far-red, red/far-red, blue/ far-red, red/blue, far-red/green, etc.) that depend on the type of algae [25]. Similar to plant phytochromes, their photosensory core module (PCM) is canonically constituted of the conserved consecutive PAS, GAF, and PHY domains. However, the output modules in the C-terminal are more diverse in their composition, with histidine kinases or related domains as well as the presence of one or more response regulator receiver (REC) domains [26]. The proteins in this family are CparGPS1, EsilPHL1, GwitGPS1, NpyrPHY1, PcolPHY1, DtenPHY1, and TastPHY1. Knowledge of the details of the functions of this type of protein will be crucial for the development of applications.
- Bacteriophytochromes (BphP) were described for the first time in the nonphotosynthetic bacterium Deinoccocus radiodurans, and over fifty have been found in purple bacteria. These proteins play important roles in intracellular signaling, regulating the expression of respiration and photosynthetic complexes. Most phytochromes are dimeric proteins, and all exhibit a modular domain of architecture PAS–GAF–PHY. This photosensory core is conserved between phytochromes in plants, bacteria, and fungi [27]. They are characterized by interacting with biliverdin IXα as an endogenous cofactor; the bilin chromophore is attached to the PAS or GAF domain. Different output domains are found on the C-terminal side of the photosensory core. In cyanobacteria and bacteria, the output module commonly consists of histidine kinase domains (PHY–histidine kinase modules), and this is the first part of a two-component signaling mechanism [28]. They have a relatively simple but diverse modular architecture that can adopt two spectroscopically different metastable states depending on the light conditions [29]. The states generated during the photocycle are generically called Pr (red light-absorbing) and Pfr (far-red light-absorbing) states. As can be seen, this denomination specifies the wavelength that stimulates the conformational changes in each bacteriophytochrome, and these wavelengths can vary between phytochrome species [30]. The complexity of the Pr→Pfr photoconversion process increases from bacteria to cyanobacteria to plants [27].
- Cyanobacterial phytochromes (Cphs) have been recognized as the most structurally and functionally diverse subgroup of the phytochrome photoreceptor superfamily. Cphs contain multiple photosensory modules that function together to fine-tune light responses [31]. The most complex type of a prokaryotic member of this family possesses a generalized photosensory module integrated by PAS–GAF–PHY domains as bacteriophytochromes [32]. However, the overall architecture of cyanobacterial phytochromes varies from the typical PAS-GAF-PHY, and some lack the upstream PAS domain while maintaining the PHY domain [33]. Cyanobacteria phytochromes use phycocyanobilin (PCB) or phytochromobilin (PΦB).
- Cyanobacteriochromes (CBCRs) are linear tetrapyrrole-binding photoreceptors with a high diversity in the colors of light they sense. Most phytochromes require an architecture composed of three domains: GAF domain (cGMP-phos- phodiesterase/adenylate cyclase/FhlA), PAS domain (Per/ARNT/Sim), and PHY domain (phytochrome-specific). CBCRs lack the PAS and PHY domains, and only the GAF domain is needed for chromophore incorporation and proper photoconversion of the CBCRs [34]. The GAF domain can attach four kinds of linear tetrapyrrole chromophores, biliverdin (BV), phytochromobilin (PFB), phycocyanobilin (PCB), and phycoviolobilin (PVB), which leads to four distinctive color-tuning mechanisms [35]. CBCRs are more spectrally diverse than phytochromes, CBCRs covering the entire UV-to-visible spectrum and near-infrared wavelengths; they function as light sensors in the 300–750 nm region [26,35].
- Xanthopsin are also called photoactive yellow proteins (PYPs), and they are characterized by the binding of the chromophore from cinnamic acid thioester- to coumarin-based ligands [36,37]. PYP is a model bacterial photoreceptor that has an evolutionary domain of the PAS superfamily [35] (Per-Arnt-Sim, named after the Per, Arnt, and Sim proteins, in which they were first observed) and is restricted to a few bacterial phyla and distinct from other PAS domains. These proteins play the role of photoreceptors for signal transduction in gene expression, motility, and biofilm formation [38]. A light-absorbing chromophore in the protein absorbs blue light and changes its shape from a nearly straight conformation (trans) to a bent conformation (cis) in less than a picosecond. Then, the activation of other sensing proteins in the bacterium occurs, which controls the direction of the bacterium. Finally, the chromophore shifts back to the straight conformation in less than a second, ready to sense another blue photon [39]. PYP-like proteins were identified first in halophilic purple bacteria, and through phylogenetic studies, they can be found in orders such as Myxococcota, Proteobacteria, and some other more distant bacterial phyla [38].
- Advantages of this type of protein include its small size, relatively high brightness, and photostability of synthetic fluorescent probes, such as the PYP from the halophilic phototrophic bacterium Halorhodospira halophila [37]. Proteins fused to tags on PYPs can be quantified due to the acquisition of a yellow color upon adding a precursor of the chromophore. The production of the target protein can be conducted via visual inspection within a few seconds, as well as with the aid of a spectrometer within a few minutes [40]. Other applications of PYPs include their employment to image proteins in a cellular environment as tags and fluorescent probes [41], films for optical switching on circuits [42], and optogenetic modules exerting allosteric regulation in a light-dependent manner [43], among others.
- Cryptochromes are photolyase-like flavoproteins that mediate blue-light regulation of gene expression and photomorphogenic responses. These receptors were originally discovered in Arabidopsis thaliana, but were later found in other plants, microbes, and animals. Despite cryptochromes being structurally related to photolyases since both are flavoproteins, only photolyases catalyze light-dependent DNA repair. On the other hand, cryptochromes have carboxyl-terminal extensions of variable length, and usually they have lost or reduced DNA repair activity and play a role in signaling. However, there are several examples of photolyases, including some from fungi, that have a dual function as a DNA-repair enzyme and photoreceptor. Genes encoding bacterial and fungal cryptochromes are found in different taxonomic groups. Very few cryptochromes from bacteria have been characterized [44]. The FeS-CPD (iron-sulfur bacterial-cryptochrome/photolyases) includes phrB from Agrobacterium. While members of the cluster CryPro (proteobacterial cryptochromes) are highly abundant in proteobacteria and cyanobacteria [45]. On the other hand, Cry-DASH proteins are capable of binding single-stranded and double-stranded DNA or RNA but do not always provide photorepair activity. Cry-DASH proteins participate in the regulation of development and pigment accumulation and the regulation of the circadian clock through a CRY-dependent oscillator [46]. CRY-DASH proteins have been found in photosynthetic cyanobacteria and also in nonphotosynthetic bacteria, fungi, plants, and animals. The shape of cryptochromes changes in response to blue-light perception from an inactive monomeric state to an active homodimeric state.
- UV-B receptors. The first protein identified of this kind is UVR8 (UV Resistance Locus 8) from Arabidopsis thaliana. For this type of protein, no homologues have been identified in bacteria or fungi; as was observed, a very low percentage of identity was identified in phylogenetic studies. The UVR8 family proteins have a highly conserved domain called VP, which is useful for the interaction of the COP1 protein, a key event in UV-B signaling. Additionally, there is a conserved peptide repeat called GWRHT (Gly-Trp-Arg-His-Thr), that generates a triad of closely packed tryptophans for UV-B photoreception [47]. Unlike other photoreceptors, UVR8 does not contain an external chromophore, but it uses tryptophan side chains to sense UV-B light. The homodimer of UVR8 dissociates into two monomers in response to UV-B irradiation, and the reaction is reversible by removing the UV-B stimulus [48]. Each monomer interacts with signaling partners to regulate the expression of genes that trigger UV protective mechanisms [49]. This behavior is useful for the design of UV-B-based optogenetic tools. Since it does not require external chromophores, it can be used in models other than plants. Optogenetic tools have been used in mammalian cells to regulate gene expression through the assembly of a chimeric transcription factor, and to localize secreted proteins of interest [50]. Furthermore, in yeast, there was a report on the expression of an activation system based on the organization of the genome [51].
- BLUF (blue-light sensors using flavin-adenine dinucleotide) proteins are flavin-nucleotide-binding cryptochromes that control enzyme activity or gene expression in response to blue light [52]. The structural element responsible for the detection of light in these photoreceptors is the BLUF domain (15 kDa); it transmits the light-induced signal to downstream protein modules via intermolecular or intramolecular interactions. Unlike other photoreception mechanisms, such as those developed by rhodopsin or phytochromes, the photoactivation of the BLUF proteins does not involve major structural changes in the chromophore FAD [53]. The interaction with the FAD chromophore is mainly mediated by nonovalent contacts between the chromophore and various amino acids of the BLUF domain; however, all BLUF proteins show conserved Tyr, Gln, and Met residues intimately related to function [52]. In particular, the signaling status of BLUF proteins arises from the structural change in the hydrogen bonding network between FAD, Gln, and Tyr, conserving the active site [54].
- Opsins are transmembrane proteins that use the retina to respond to different light bands in the UV-to-red spectral region. These proteins have different functions, such as the control of proton gradients, the maintenance of membrane potential, ionic homeostasis, and the modulation of flagellar motor rotation. Opsins can be found across all kingdoms of life, and they require the incorporation of a vitamin A-related organic photon-absorbing cofactor to enable light sensitivity, a complex referred to as rhodopsin [55]. Opsin genes are divided into two families: microbial opsins (type I) and animal opsins (type II). Even though no sequence similarity is shared between microbial and animal rhodopsins, they share a common architecture of seven transmembrane α-helices (TM) with the N- and C-terminus facing out- and inside the cell, respectively. Most microbial rhodopsins function as light-sensing receptors and light-driven ion pumps for the active transport of ions (H+, Na+, Cl−, etc.). On the other hand, some microbial rhodopsins function as light-gated ion channels, also called channelrhodopsins, mainly used as optogenetic tools in neuroscience.
3. Bioluminescent Proteins
4. Photoswitchable Proteins
4.1. Photoswitching Mechanism of Bacteriophytochromes
4.2. Photoswitching Mechanism of LOV Domain Proteins
4.3. Photoswitching Mechanism of BLUF Domain Proteins
5. Novel Applications
5.1. NIR-Based Imaging
5.2. Optogenetics
5.3. Optoprotein-Based Materials
5.4. Bioluminescence to Detect Pollutants
5.5. Intensification of Bioprocesses Based on the Optocontrol
Bioprocess to Control | Micro-Organism | Optogenetic System | Importance | Ref. |
---|---|---|---|---|
Mevalonate and isobutanol production at 2 L bioreactor scale | Escherichia coli | OptoLAC circuit based on the control of lacI by the PR promoter of the pDawn system. The blue light was used to control the process. | Production was significantly increased compared with a traditional IPTG system of genetic control. The OptoLAC circuit can be used in other applications for E. coli currently based on IPTG induction. | [166] |
The programmable assembly/disassembly of membraneless organelles | Saccharomyces cerevisiae | PixELLs optocontrol system | The control of engineered metabolic pathways by assembly and disassembly of metabolically active enzymes clusters. | [167] |
Ethanol and isobutanol bioproduction | Saccharomyces cerevisiae | OptoINVRT-ILV2 (Ethanol) and OptoEXPPDC1 (Isobutanol). The blue light was used to control the process. | It offers an option to delete essential pathways that compete with the pathway of the interest bioproduct. | [164] |
Induction of the autoflocculation process of yeast. | Saccharomyces cerevisiae | Light control of the flocculin-encoding gene FLO1 by the FUN-LOV optocontrol system | It offers a low-cost alternative to typical bioseparation performed by membranes. | [124] |
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Name | Kingdom | Chromophore | Excitation Wavelength | Reversion Wavelength | Type |
---|---|---|---|---|---|
Am1 c0023g2/BAm | bacteria | Phycocyanobilin | 680 nm | 525 nm | Cyanobacteriochrome |
PixD/PixE | bacteria | FAD/FMN | 450 nm | dark | BLUF |
BcLOV4 | fungi | FMN | 450 nm | dark | LOV |
EL222 | bacteria | FMN | 450 nm | dark | LOV |
pMag/nMag | fungi | FAD | 450 nm | dark | LOV |
NcWC1-LOV | fungi | FAD | 450 nm | dark | LOV |
RsLOV | bacteria | FMN | 450 nm | dark | LOV |
VVD | fungi | FMN/FAD | 450 nm | dark | LOV |
YtvA | bacteria | FMN/FAD/RF | 450 nm | dark | LOV |
PYP | bacteria | p-coumaric acid | 450 nm | dark | fluorescent |
MxCBD | bacteria | AdoCbl, MetCbl or CNCbl | 545 nm | dark | cobalamin-binding |
TtCBD | bacteria | AdoCbl, MetCbl or CNCbl | 545 nm | dark | cobalamin-binding |
BphP1/PpsR2 | bacteria | biliverdin | 760 nm | 640 nm/dark | phytochromes |
BphP1/Q-PAS1 | bacteria | biliverdin | 760 nm | 640 nm/dark | phytochromes |
Cph1 | bacteria | PCB | 660 nm | 740 nm | phytochromes |
DrBphP | bacteria | biliverdin | 660 nm | 780 nm/dark | phytochromes |
iLight | bacteria | biliverdin | 660 nm | 760 nm | phytochromes |
MagRed | bacteria | biliverdin | 660 nm | 780 nm/dark | phytochromes |
NIR-FPs | Ex/Em (nm) and Organization | Properties | Bacterial Phytochrome Template | Ref. |
---|---|---|---|---|
IFP1.4 | 684/708 nm monomeric and dimeric. | It expresses well in mammalian cells and mice. It does not fluoresce without a BV supply. It is the brighter version of IFP2.0. | Designed from DrBphP (Deinococcus radiodurans). It has a truncation of the PHY and C-terminal histidine kinase–related domains and underwent mutagenesis. | [109] |
Wi-Phy | 701/719 nm monomeric | Its application in cells or animals has not been demonstrated. | A variant of the Deinococcus radiodurans DrCBD-D207H with Y263F | [108] |
IFP1.4rev | 685/708 nm | It presents high brightness and a large complementation contrast, but it is irreversible. Applicable for in vivo protein-protein interaction studies. | Arose from protein IFP1.4 with the mutation H207D. | [107] |
iRFP713 | 690/713 nm dimeric | It is stable, noncytotoxic, and the low concentrations of endogenous BV are sufficient to make it brightly fluorescent in cells, tissues, and whole animals. | Generated from RpBphP2 from the photosynthetic bacterium Rhodopseudomonas palustris. | [110] |
iSplit | 690/713 nm separate domains | Configuration suitable as a reporter. Based on bimolecular fluorescence complementation (BiFC). Allows detection of interactions in vivo. | Produced by separating iRFP713 into individual PAS and GAF domains using directed mutagenesis. | [111] |
iRFP670 iRFP682 iRFP702 iRFP720 | 643/670 nm 663/683 nm 673/702 nm 702/720 nm dimeric | Proteins with high effective brightness and low cytotoxicity in vitro and in vivo, without the addition of exogenous BV. Efficient two-color imaging in living mice. Can mainly serve for labeling of organelles and whole cells. Multicolor microscopy and whole-body imaging, photoacoustic tomography, fluorescence lifetime imaging, tumors and metastases. | Developed by mutagenesis of RpBphP6 and RpBphP2. RpBphP6 was cut to only have PAS and GAF domains, and the mutations D202 and Y258F. Finally, several rounds of random mutagenesis were performed. | [112] |
miRFPs: miRFP670 miRFP703 miRFP709 | 642/670 nm 673/703 nm 683/709 nm monomeric | It fully relies on endogenous BV to fluoresce. miRFPs make it possible to create NIR biosensors for tasks like monitoring protein-protein interactions and other applications. They demonstrate excellent performance in microscopy, flow cytometry, and whole-body imaging. | Consists of mutated AS-GAF domains (first 315 amino acids) of RpBphP1 from Rhodopseudomonas palustris. | [113] |
BphP1 | Ex. 780 nm Em. none Max.Abs. Pfr (ON) 756 nm Pr (OFF) 678 nm monomeric | BphP1 exhibits the most significant red-shifted absorption compared to other BphPs. BphP1 has two red- and NIR-absorbing photoconvertible states, enabling photoacoustic imaging and the ability to switch between states in deep tissues. | Full-length phytochrome RpBphP1 from the bacterium Rhodopseudomonas palustris (~82 kDa) | [114] |
mIFP | 683/704 nm monomeric | mIFP effectively labels proteins in live cells without any apparent harmful effects. However, when employed in vivo, it necessitates the introduction of an external cofactor. | Modification of BrBphP from Bradyrhizobium with site-specific mutagenesis, DNA shuffling and random mutagenesis. | [115] |
PAiRFP1 PAiRFP2 | 690/717 nm 692/719 nm dimeric | The weakly fluorescent PAiRFPs undergo photoconversion transforming into a strongly fluorescent state upon excitation. After photoactivation, PAiRFPs gradually return to their original state, allowing for numerous cycles of photoactivation and relaxation. | Molecular evolution of BphP from Agrobacterium tumefaciens C58, called AtBphP2. | [116] |
Optoprotein | Microorganism | Functionalization Technique | Photoreceptor | Material | Wavelength | Application | Ref. |
---|---|---|---|---|---|---|---|
EL222 | Erythrobacter litoralis | Thiol-malemide |
EL222
Homomerization | Collagen hydrogel |
450 nm
Dark reversible | Enhance crossliking, improve mechanical properties for cell proliferation | [157] |
CarHC | Pectobacterium carotovorum | Spy chemistry | CarHCc Oligomerization | Elastin-like polypeptide (ELP) | 522 nm Dark reversible | Cell/protein control release and improvement of mechanical properties | [147,158] |
Cph1 | Synechocystis sp. PCC 6803 | Michael-type addition and Histidine Tag | Cph1 Homodimerization | PEG-VS hydrogel | 660 nm 740 reversible | Mechanical properties | [144,145] |
VVD | Neurospora crassa | Histidine Tag | VVD homodimerization | Ni 2+ NTA colloidal particles | 450 nm and 660 nm Dark reversible | Self-sorting /Self-assembly of colloidal particles | [145] |
PYP | Halorhodospira halophila | Film deposition | Intramolecular conformational change | Mach–Zehnder interferometer | 445 nm Dark reversible | Improve optical characteristics of IO circuits | [42] |
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Ramírez Martínez, C.; Gómez-Pérez, L.S.; Ordaz, A.; Torres-Huerta, A.L.; Antonio-Perez, A. Current Trends of Bacterial and Fungal Optoproteins for Novel Optical Applications. Int. J. Mol. Sci. 2023, 24, 14741. https://doi.org/10.3390/ijms241914741
Ramírez Martínez C, Gómez-Pérez LS, Ordaz A, Torres-Huerta AL, Antonio-Perez A. Current Trends of Bacterial and Fungal Optoproteins for Novel Optical Applications. International Journal of Molecular Sciences. 2023; 24(19):14741. https://doi.org/10.3390/ijms241914741
Chicago/Turabian StyleRamírez Martínez, Carolina, Leonardo S. Gómez-Pérez, Alberto Ordaz, Ana Laura Torres-Huerta, and Aurora Antonio-Perez. 2023. "Current Trends of Bacterial and Fungal Optoproteins for Novel Optical Applications" International Journal of Molecular Sciences 24, no. 19: 14741. https://doi.org/10.3390/ijms241914741