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Responding to light signals: a comprehensive update on photomorphogenesis in cyanobacteria

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Abstract

Cyanobacteria are ancestors of chloroplast and perform oxygen-evolving photosynthesis similar to higher plants and algae. However, an obligatory requirement of photons for their growth results in the exposure of cyanobacteria to varying light conditions. Therefore, the light environment could act as a signal to drive the developmental processes, in addition to photosynthesis, in cyanobacteria. These Gram-negative prokaryotes exhibit characteristic light-dependent developmental processes that maximize their fitness and resource utilization. The development occurring in response to radiance (photomorphogenesis) involves fine-tuning cellular physiology, morphology and metabolism. The best-studied example of cyanobacterial photomorphogenesis is chromatic acclimation (CA), which allows a selected number of cyanobacteria to tailor their light-harvesting antenna called phycobilisome (PBS). The tailoring of PBS under existing wavelengths and abundance of light gives an advantage to cyanobacteria over another photoautotroph. In this work, we will provide a comprehensive update on light-sensing, molecular signaling and signal cascades found in cyanobacteria. We also include recent developments made in other aspects of CA, such as mechanistic insights into changes in the size and shape of cells, filaments and carboxysomes.

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References

  • Abe K, Miyake K et al (2014) Engineering of a green-light inducible gene expression system in Synechocystis sp. PCC 6803. Microb Biotechnol 7(2):177–183

    Article  CAS  PubMed  Google Scholar 

  • Agostoni M, Montgomery BL (2014) Survival strategies in the aquatic and terrestrial world: the impact of second messengers on cyanobacterial processes. Life 4:745–769

    Article  PubMed  PubMed Central  Google Scholar 

  • Agostoni M, Koestler BJ et al (2013) Occurrence of cyclic di-GMP-modulating output domains in cyanobacteria: an illuminating perspective. mBio 4:e00451–13

  • Alvey RM, Karty JA et al (2003) Lesions in phycoerythrin chromophore biosynthesis in Fremyella diplosiphon reveal coordinated light regulation of apoprotein and pigment biosynthetic enzyme gene expression. Plant Cell 15:2448–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders K, Daminelli-Widany G et al (2013) Structure of the cyanobacterial phytochrome 2 photosensor implies a tryptophan switch for phytochrome signaling. J Biol Chem 288:35714–35725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ariyanti D, Ikebukuro K, Sode K (2021) Artificial complementary chromatic acclimation gene expression system in Escherichia coli. Microb Cell Fact 20:128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babin M, Stramski D et al (2003) Variations in the light absorption coefficients of phytoplankton, non-algal particles, and dissolved organic matter in coastal waters around Europe. J Geophys Res Oceans. https://doi.org/10.1029/2001JC000882

    Article  Google Scholar 

  • Badger MR, Price GD (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol Plant 84:606–615

    Article  CAS  Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622

    Article  CAS  PubMed  Google Scholar 

  • Balabas BE, Montgomery BL et al (2003) CotB is essential for complete activation of green light-induced genes during complementary chromatic adaptation in Fremyella diplosiphon. Mol Microbiol 50:781–793

    Article  CAS  PubMed  Google Scholar 

  • Beardall J, Stojkovic S, Larsen S (2009) Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205

    Article  Google Scholar 

  • Bebout BM, Garcia-Pichel F (1995) UV B-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61(12):4215–4222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrenfeld MJ, O’Malley RT et al (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755

    Article  CAS  PubMed  Google Scholar 

  • Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58(2):419–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bezy RP, Kehoe DM (2010) Functional characterization of a cyanobacterial OmpR/PhoB class transcription factor binding site controlling light color responses. J Bacteriol 192:5923–5933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhaya D (2016) In the limelight: photoreceptors in cyanobacteria. mBio 7(3):e00741–16

  • Bhaya D, Takahashi A, Grossman AR (2001) Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 98:7540–7545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bittencourt-Oliveira MDC, Buch B et al (2012) Effects of light intensity and temperature on Cylindrospermopsis raciborskii (cyanobacteria) with straight and coiled trichomes: growth rate and morphology. Braz J Biol 72:343–351

    Article  CAS  PubMed  Google Scholar 

  • Bordowitz JR, Montgomery BL (2008) Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon. J Bacteriol 190(11):4069–4074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brudler R, Hitomi K et al (2003) Identification of a new cryptochrome class: structure, function, and evolution. Mol Cell 11(1):9–67

    Article  Google Scholar 

  • Buchberger T, Lamparter T (2015) Streptophyte phytochromes exhibit an N-terminus of cyanobacterial origin and a C-terminus of proteobacterial origin. BMC Res Notes 8:1–13

    Article  CAS  Google Scholar 

  • Burgie ES, Bussell AN et al (2014) Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proc Natl Acad Sci USA 111:10179–10184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch AW, Montgomery BL (2015) The tryptophan-rich sensory protein (TSPO) is involved in stress-related and light-dependent processes in the cyanobacterium Fremyella diplosiphon. Front Microbiol 6:1393

    Article  PubMed  PubMed Central  Google Scholar 

  • Butler WL, Norris KH et al (1959) Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci USA 45:1703–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calzadilla PI, Kirilovsky D (2020) Revisiting cyanobacterial state transitions. Photochem Photobiol Sci 19(5):585–603

    Article  CAS  PubMed  Google Scholar 

  • Campbell D (1996) Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142:1255–1263

    Article  CAS  PubMed  Google Scholar 

  • Campbell D, Houmard J, de Marsac NT (1993) Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix. Plant Cell 5(4):451–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell D, Eriksson M-J et al (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci USA 95:364–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell EL, Hagen KD et al (2015) Genetic analysis reveals the identity of the photoreceptor for phototaxis in hormogonium filaments of Nostoc punctiforme. J Bacteriol 197:782–791

    Article  PubMed  PubMed Central  Google Scholar 

  • Casey ES, Grossman AR (1994) In vivo and in vitro characterization of the light-regulated cpcB2A2 promoter of Fremyella diplosiphon. J Bacteriol 176:6362–6374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cashmore AR, Jarillo JA et al (1999) Cryptochromes: blue light receptors for plants and animals. Science 284(5415):760–765

    Article  CAS  PubMed  Google Scholar 

  • Castenholz RW, Garcia-Pichel F (2012) Cyanobacterial responses to UV-radiation. In: Whitton BA (ed) The ecology of cyanobacteria II: their diversity in space and time. Kluwer Academic Publishers, Dordrecht, pp 481–499

    Chapter  Google Scholar 

  • Chavan AG, Swan JA et al (2021) Reconstitution of an intact clock reveals mechanisms of circadian timekeeping. Science 374(6564):eabd4453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chazan A, Das I et al (2023) Phototrophy by antenna-containing rhodopsin pumps in aquatic environments. Nature 615:535–540

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117

    Article  CAS  PubMed  Google Scholar 

  • Chiang GG, Schaefer MR, Grossman AR (1992) Complementation of a red-light-indifferent cyanobacterial mutant. Proc Natl Acad Sci USA 89(20):9415–9419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chukhutsina VU, van Thor JJ (2022) Molecular activation mechanism and structural dynamics of orange carotenoid protein. Physchem 2(3):235–252

    Article  CAS  Google Scholar 

  • Chuon K, Shim JG et al (2023) Natural selection of carotenoid binding in Gloeobacter rhodopsin. Algal Res 74:103232

    Article  Google Scholar 

  • Cobley JG, Miranda RD (1983) Mutations affecting chromatic adaptation in the cyanobacterium Fremyella diplosiphon. J Bacteriol 153(3):1486–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobley JG, Zerweck E et al (1993) Construction of shuttle plasmids which can be efficiently mobilized from Escherichia coli into the chromatically adapting cyanobacterium, Fremyella diplosiphon. Plasmid 30:90–105

    Article  CAS  PubMed  Google Scholar 

  • Cobley JG, Clark AC et al (2002) CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol Microbiol 44(6):1517–1531

    Article  CAS  PubMed  Google Scholar 

  • Conley PB, Lemaux PG, Grossman AR (1985) Cyanobacterial light-harvesting complex subunits encoded in two red light induced transcripts. Science 230:550–553

    Article  CAS  PubMed  Google Scholar 

  • Conley PB, Lemaux PG et al (1986) Genes encoding major light harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad Sci USA 83:3924–3928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conley PB, Lemaux PG, Grossman AR (1988) Molecular characterization and evolution of sequences encoding light-harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon. J Mol Biol 199:447–465

    Article  CAS  PubMed  Google Scholar 

  • Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42(1):2–10

    Article  CAS  PubMed  Google Scholar 

  • de Marsac NT (1983) Phycobilisomes and complementary chromatic adaptation in cyanobacteria. Bull Inst Pasteur 81(3):201–254

    Google Scholar 

  • de Marsac NT, Cohen-Bazire G (1977) Molecular composition of cyanobacterial phycobilisomes. Proc Natl Acad Sci USA 74:1635–1639

    Article  PubMed  PubMed Central  Google Scholar 

  • Domínguez-Martín MA, Sauer PV et al (2022) Structures of a phycobilisome in light-harvesting and photoprotected states. Nature 609(7928):835–845

    Article  PubMed  Google Scholar 

  • Dwijayanti A, Zhang, et al (2022) Toward multiplexed optogenetic circuits. Front Bioeng Biotechnol 9:804563

    Article  PubMed  PubMed Central  Google Scholar 

  • Engelmann TW (1883) Farbe und assimilation. Assimilation findet nur in den farbstoffhaltigen plasmathielchen statt II Näherer zusamennhang zwischen lichtabsorption und assimilation. Bot Z 41:1–13

    Google Scholar 

  • Engelmann TW (1902) Untersuchungen über die qualitativen beziehungen zwieschen absorbtion des lichtes und assimilation in pflanzenzellen. I. Das mikrospectraphotometer, ein apparat zur qualitativen mikrospectralanalyse. II. Experimentelle grundlangen zur ermittelung der quantitativen beziehungen zwieschen assimilationsenergie und absorptiongrösse. III. Bestimmung der vertheilung der energie im spectrum von sonnenlicht mittels bacterienmethode und quantitativen mikrospectralanalyse. Bot Z 42:81–105

    Google Scholar 

  • Enomoto G, Nomura R et al (2014) Cyanobacteriochrome SesA is a diguanylate cyclase that induces cell aggregation in Thermosynechococcus. J Biol Chem 289:24801–24809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enomoto G, Ni-Ni-Win et al (2015) Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. Proc Natl Acad Sci USA 112:8082–8087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enomoto G, Wallner T, Wilde A (2023) Control of light-dependent behaviour in cyanobacteria by the second messenger cyclic di-GMP. Microlife 4:uqad019

    Article  PubMed  PubMed Central  Google Scholar 

  • Everroad C, Six C et al (2006) Biochemical bases of type IV chromatic adaptation in marine Synechococcus sp. J Bacteriol 188(9):3345–3356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang M, Chavan AG et al (2023) Synchronization of the circadian clock to the environment tracked in real time. Proc Natl Acad Sci USA 120(13):e2221453120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federspiel NA, Grossman AR (1990) Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bacteriol 172:4072–4081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federspiel NA, Scott L (1992) Characterization of a light-regulated gene encoding a new phycoerythrin-associated linker protein from the cyanobacterium Fremyella diplosiphon. J Bacteriol 174:5994–5998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiedler B, Broc D et al (2004) Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol 79:551–555

    Article  CAS  PubMed  Google Scholar 

  • Freire P, Moreira RN, Arraiano CM (2009) BolA inhibits cell elongation and regulates MreB expression levels. J Mol Biol 385:1345–1351

    Article  CAS  PubMed  Google Scholar 

  • Fushimi K, Narikawa R (2019) Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum. Curr Opin Struct Biol 57:39–46

    Article  CAS  PubMed  Google Scholar 

  • Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17(10):3450–3465

    Article  CAS  PubMed  Google Scholar 

  • Gan F, Zhang S et al (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317

    Article  CAS  PubMed  Google Scholar 

  • Gendel S, Ohad I, Bogorad L (1979) Control of phycoerythrin synthesis during chromatic adaptation. Plant Physiol 64(5):786–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gisriel CJ, Elias E et al (2023) Helical allophycocyanin nanotubes absorb far-red light in a thermophilic cyanobacterium. Sci Adv 9(12):eadg0251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glass JB, Kretz CB et al (2015) Current perspectives on microbial strategies for survival under extreme nutrient starvation: evolution and ecophysiology. In: Bakermans C (ed) Microbial evolution under extreme conditions. De Gruyter, Berlin, pp 127–152

    Chapter  Google Scholar 

  • Gorelova OA, Baulina OI et al (2013) The pleiotropic effects of ftn2 and ftn6 mutations in cyanobacterium Synechococcus sp. PCC 7942: an ultrastructural study. Protoplasma 250:931–942

    Article  CAS  PubMed  Google Scholar 

  • Gutu A, Kehoe DM (2012) Emerging perspectives on the mechanisms, regulation, and distribution of light color acclimation in cyanobacteria. Mol Plant 5(1):1–13

    Article  CAS  PubMed  Google Scholar 

  • Gutu A, Nesbit AD et al (2013) Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression. Proc Natl Acad Sci USA 110(40):16253–16258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He YY, Häder D-P (2002) Reactive oxygen species and UV-B: effect on cyanobacteria. Photochem Photobiol Sci 1:729–736

    Article  CAS  PubMed  Google Scholar 

  • Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7(4):263–273

    Article  CAS  PubMed  Google Scholar 

  • Hirose Y, Shimada T et al (2008) Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. Proc Natl Acad Sci USA 105:9528–9533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose Y, Narikawa R et al (2010) Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. Proc Natl Acad Sci USA 107:8854–8859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose Y, Rockwell NC et al (2013) Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proc Natl Acad Sci USA 110:4974–4979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houmard J, Capuano V et al (1988) Genes encoding core components of the phycobilisome in the cyanobacterium Calothrix sp. strain PCC 7601: occurrence of a multigene family. J Bacteriol 170:5512–5521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houmard J, Capuano V et al (1990) Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes. Proc Natl Acad Sci USA 87:2152–2156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Yang G et al (2007) MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 63:1640–1652

    Article  CAS  PubMed  Google Scholar 

  • Hwang DY, Park S et al (2019) GIGANTEA regulates the timing stabilization of CONSTANS by altering the interaction between FKF1 and ZEITLUPE. Mol Cells 42(10):693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeuchi M, Ishizuka T (2008) Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem Photobiol Sci 7:1159–1167

    Article  CAS  PubMed  Google Scholar 

  • Imasheva ES, Balashov SP et al (2009) Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna. Biochemistry 48(46):10948–10955

    Article  CAS  PubMed  Google Scholar 

  • Ishizuka T, Shimada T et al (2006) Characterization of cyanobacteriochrome TePixJ from a thermophilic cyanobacterium Thermosynechococcus elongatus strain BP-1. Plant Cell Physiol 47(9):1251–1261

    Article  CAS  PubMed  Google Scholar 

  • Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431

    Article  CAS  PubMed  Google Scholar 

  • Jing Y, Lin R (2020) Transcriptional regulatory network of the light signaling pathways. New Phytol 227(3):683–697

    Article  CAS  PubMed  Google Scholar 

  • Jung KH, Trivedi VD, Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47:1513–1522

    Article  CAS  PubMed  Google Scholar 

  • Kahn K, Mazel D et al (1997) A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. J Bacteriol 179:998–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kehoe DM, Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412

    Article  CAS  PubMed  Google Scholar 

  • Kehoe DM, Grossman AR (1997) New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J Bacteriol 179:3914–3921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kehoe DM, Grossman AR (1998) Use of molecular genetics to investigate complementary chromatic adaptation: advances in transformation and complementation. Methods Enzymol 297:279–290

    Article  CAS  Google Scholar 

  • Kehoe DM, Gutu A (2006) Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57:127–150

    Article  CAS  PubMed  Google Scholar 

  • Khayatan B, Meeks JC, Risser DD (2015) Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria. Mol Microbiol 98(6):1021–1036

    Article  CAS  PubMed  Google Scholar 

  • Koksharova OA, Klint J, Rasmussen U (2007) Comparative proteomics of cell division mutants and wild-type of Synechococcus sp. strain PCC 7942. Microbiology 153(8):2505–2517

    Article  CAS  PubMed  Google Scholar 

  • Kronfel CM, Hernandez CV 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(11):3987–3999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar K, Mella-Herrera RA et al (2010) Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2(4):a000315

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar V, Maurya PK et al (2019) Photomorphogenesis in the cyanobacterium Fremyella diplosiphon improves photosynthetic efficiency. In: Mishra AK, Tiwari DN, Rai AN (eds) Cyanobacteria. Academic Press, Elsevier Inc., San Diego, pp 131–143

    Chapter  Google Scholar 

  • Kupriyanova EV, Pronina NA, Los DA (2023) Adapting from low to high: an update to CO2-concentrating mechanisms of cyanobacteria and microalgae. Plants 12(7):1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb JJ, Røkke G, Hohmann-Marriott MF (2018) Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica 56(1):105–124

    Article  CAS  Google Scholar 

  • Leister D (2023) Enhancing the light reactions of photosynthesis: strategies, controversies, and perspectives. Mol Plant 16(1):4–22

    Article  CAS  PubMed  Google Scholar 

  • Li L, Kehoe DM (2005) In vivo analysis of the roles of conserved aspartate and histidine residues within a complex response regulator. Mol Microbiol 55:1538–1552

    Article  CAS  PubMed  Google Scholar 

  • Liu TS, Wu KF et al (2023) Identification of a far-red light-inducible promoter that exhibits light intensity dependency and reversibility in a cyanobacterium. ACS Synth Biol 12(4):1320–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Losi A, Polverini E et al (2002) First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys J 82(5):2627–2634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mantovani O, Haffner M et al (2023) Roles of second messengers in the regulation of cyanobacterial physiology: the carbon-concentrating mechanism and beyond. Microlife 4:uqad008

    Article  PubMed  PubMed Central  Google Scholar 

  • Mascher T, Helmann JD, Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70(4):910–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mascoli V, Bhatti AF et al (2022) The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II. Nat Commun 13(1):3562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masuda S (2013) Light detection and signal transduction in the BLUF photoreceptors. Plant Cell Physiol 54(2):171–179

    Article  CAS  PubMed  Google Scholar 

  • Masuda S, Hasegawa K et al (2004) Light-induced structural changes in a putative blue-light receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of Synechocystis sp. PCC 6803. Biochemistry 43(18):5304–5313

    Article  CAS  PubMed  Google Scholar 

  • Maurya PK, Mondal S et al (2021) Roadmap to sustainable carbon-neutral energy and environment: can we cross the barrier of biomass productivity? Environ Sci Pollut Res 28:49327–49342

    Article  Google Scholar 

  • Maurya PK, Kumar V et al (2022) Chromatic acclimation in cyanobacteria: photomorphogenesis in response to light quality. In: Rastogi RP (ed) Ecophysiology and biochemistry of cyanobacteria. Springer Singapore, Singapore, pp 209–223

    Google Scholar 

  • Maurya PK, Mondal S et al (2023) Green and blue light-dependent morphogenesis, decoupling of phycobilisomes and higher accumulation of reactive oxygen species and lipid contents in Synechococcus elongatus PCC 7942. Environ Exp Bot 205:105105

    Article  CAS  Google Scholar 

  • Mazel D, Guglielmi G et al (1986) Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res 14:8279–8290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McConnell MD, Koop R et al (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130(3):1201–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery BL (2007) Sensing the light: photoreceptive systems and signal transduction in cyanobacteria. Mol Microbiol 64(1):16–27

    Article  CAS  PubMed  Google Scholar 

  • Montgomery BL (2015) Light-dependent governance of cell shape dimensions in cyanobacteria. Front Microbiol 6:514

    Article  PubMed  PubMed Central  Google Scholar 

  • Montgomery BL (2016) Mechanisms and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria. J Exp Bot 67(14):4079–4090

    Article  CAS  PubMed  Google Scholar 

  • Montgomery BL (2022) Reflections on cyanobacterial chromatic acclimation: exploring the molecular bases of organismal acclimation and motivation for rethinking the promotion of equity in STEM. Microbiol Mol Biol Rev 86(3):e00106-e121

    Article  PubMed  PubMed Central  Google Scholar 

  • Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7(8):357–366

    Article  CAS  PubMed  Google Scholar 

  • Moon YJ, Park YM et al (2004) Calcium is involved in photomovement of cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol 79:114–119

    Article  CAS  PubMed  Google Scholar 

  • Moon YJ, Kim SY et al (2011) Cyanobacterial phytochrome Cph2 is a negative regulator in phototaxis toward UV-A. FEBS Lett 585:335–334

    Article  CAS  PubMed  Google Scholar 

  • Muzzopappa F, Kirilovsky D (2020) Changing color for photoprotection: the orange carotenoid protein. Trends Plant Sci 25(1):92–104

    Article  CAS  PubMed  Google Scholar 

  • Nakajima M, Ferri S et al (2016) Construction of a miniaturized chromatic acclimation sensor from cyanobacteria with reversed response to a light signal. Sci Rep 6(1):37595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakasone Y, Murakami H et al (2023) Time-resolved study on signaling pathway of photoactivated adenylate cyclase and its nonlinear optical response. J Biol Chem 299:105285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narikawa R, Okamoto S et al (2008) Molecular evolution of PAS domain-containing proteins of filamentous cyanobacteria through domain shuffling and domain duplication. DNA Res 11(2):69–81

    Article  Google Scholar 

  • Narikawa R, Suzuki F et al (2011) Novel photosensory two-component system (PixA-NixB-NixC) involved in the regulation of positive and negative phototaxis of cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 52:2214–2224

    Article  CAS  PubMed  Google Scholar 

  • Neunuebel MR, Golden JW (2008) The Anabaena sp. strain PCC 7120 gene all2874 encodes a diguanylate cyclase and is required for normal heterocyst development under high-light growth conditions. J Bacteriol 190(20):6829–6836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng WO, Grossman AR, Bhaya D (2003) Multiple light inputs control phototaxis in Synechocystis sp. strain PCC 6803. J Bacteriol 185:1599–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oelmüller R, Conley PB et al (1988) Changes in accumulation and synthesis of transcripts encoding phycobilisome components during acclimation of Fremyella diplosiphon to different light qualities. Plant Physiol 88:1077–1083

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohlendorf R, Möglich A (2022) Light-regulated gene expression in bacteria: fundamentals, advances, and perspectives. Front Bioeng Biotechnol 10:1029403

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohmori M, Okamoto S (2004) Photoresponsive cAMP signal transduction in cyanobacteria. Photochem Photobiol Sci 3:503–511

    Article  CAS  PubMed  Google Scholar 

  • Ohmori M, Terauchi K et al (2002) Regulation of cAMP-mediated photosignaling by a phytochrome in the cyanobacterium Anabaena cylindrica. Photochem Photobiol 75:675–679

    Article  CAS  PubMed  Google Scholar 

  • Okajima K, Fukushima Y et al (2006) Fate determination of the flavin photoreceptions in the cyanobacterial blue light receptor TePixD (Tll0078). J Mol Biol 363:10–18

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Kasahara M et al (2004) A phytochrome-like protein AphC triggers the cAMP signaling induced by far-red light in the cyanobacterium Anabaena sp. strain PCC 7120. Photochem Photobiol 80:429–433

    CAS  PubMed  Google Scholar 

  • Opel F, Siebert NA et al (2022) Generation of synthetic shuttle vectors enabling modular genetic engineering of cyanobacteria. ACS Synth Biol 11(5):1758–1771

    Article  CAS  PubMed  Google Scholar 

  • Pattanaik B, Montgomery BL (2010) A novel role for a TonB-family protein and photoregulation of iron acclimation in Fremyella diplosiphon. Plant Signal Behav 5:851–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattanaik B, Whitaker MJ, Montgomery BL (2012) Light quantity affects the regulation of cell shape in Fremyella diplosiphon. Front Microbiol 3:170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattanaik B, Busch AW et al (2014) Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon. Microbiology 160(5):992–1005

    Article  CAS  PubMed  Google Scholar 

  • Peleato ML, Teresa Bes M, Fillat MF (2016) Iron homeostasis and environmental responses in cyanobacteria: regulatory networks involving Fur. In: de Bruijn FJ (ed) Stress and environmental regulation of gene expression and adaptation in bacteria. Wiley Blackwell, Hoboken, pp 1065–1078

    Chapter  Google Scholar 

  • Portwich A, Garcia-Pichel F (2000) A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC 6912. Photochem Photobiol 71(4):493–498

    Article  CAS  PubMed  Google Scholar 

  • Postius C, Neuschaefer-Rube O et al (2001) N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance. FEMS Microbiol Ecol 37(2):117–125

    Article  CAS  Google Scholar 

  • Priyadarshini N, Steube N et al (2023) Evidence for an early green/red photocycle that precedes the diversification of GAF domain photoreceptor cyanobacteriochromes. Photochem Photobiol Sci 22(6):1415–1427

    Article  CAS  PubMed  Google Scholar 

  • Raven JA (2003) Carboxysomes and peptidoglycan walls of cyanelles: possible physiological functions. Eur J Phycol 38:47–53

    Article  Google Scholar 

  • Rillema R, Hoang Y et al (2021) Carboxysome mispositioning alters growth, morphology, and rubisco level of the cyanobacterium Synechococcus elongatus PCC 7942. mBio 12(4):e02696–20

  • Rockwell NC, Lagarias JC (2010) A brief history of phytochromes. ChemPhysChem 11:1172–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rockwell NC, Lagarias JC (2017) Phytochrome diversification in cyanobacteria and eukaryotic algae. Curr Opin Plant Biol 37:87–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rockwell NC, Lagarias JC (2020) Phytochrome evolution in 3D: deletion, duplication, and diversification. New Phytol 225(6):2283–2300

    Article  PubMed  Google Scholar 

  • Rockwell NC, Martin SS et al (2011) Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. Proc Natl Acad Sci USA 108(29):11854–11859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rockwell NC, Duanmu D et al (2014) Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA 111:3871–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohnke BA, Singh SP et al (2018) RcaE-dependent regulation of carboxysome structural proteins has a central role in environmental determination of carboxysome morphology and abundance in Fremyella diplosiphon. mSphere 3(1):e00617–17

  • Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639

    Article  PubMed  Google Scholar 

  • Rosinski J, Hainfeld JF et al (1981) Phycobilisome ultrastructure and chromatic adaptation in Fremyella diplosiphon. Ann Bot 47:1–12

    Article  Google Scholar 

  • Sánchez-Baracaldo P, Bianchini G et al (2022) Cyanobacteria and biogeochemical cycles through Earth history. Trends Microbiol 30(2):143–157

    Article  PubMed  Google Scholar 

  • Sanfilippo JE, Garczarek L et al (2019) Chromatic acclimation in cyanobacteria: a diverse and widespread process for optimizing photosynthesis. Annu Rev Microbiol 73:407–433

    Article  CAS  PubMed  Google Scholar 

  • Schepens I, Duek P, Fankhauser C (2004) Phytochrome-mediated light signalling in Arabidopsis. Curr Opin Plant Biol 7(5):564–569

    Article  CAS  PubMed  Google Scholar 

  • Seib LO, Kehoe DM (2002) A turquoise mutant genetically separates expression of genes encoding phycoerythrin and its associated linker peptides. J Bacteriol 184(4):962–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sineshchekov OA, Trivedi VD et al (2005) Photochromicity of Anabaena sensory rhodopsin, an atypical microbial receptor with a cis-retinal light-adapted form. J Biol Chem 280:14663–14668

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Montgomery BL (2011) Temporal responses of wild-type pigmentation and RcaE-deficient strains of Fremyella diplosiphon during light transitions. Commun Integr Biol 4(5):503–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh SP, Montgomery BL (2012) Reactive oxygen species are involved in the morphology-determining mechanism of Fremyella diplosiphon cells during complementary chromatic adaptation. Microbiology 158:2235–2245

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Montgomery BL (2014) Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon. Mol Microbiol 93:167–182

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Montgomery BL (2015) Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon. Front Microbiol 6:1215

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh SP, Häder D-P, Sinha RP (2010) Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res Rev 9(2):79–90

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Miller HL, Montgomery BL (2013) Temporal dynamics of changes in reactive oxygen species (ROS) levels and cellular morphology are coordinated during complementary chromatic acclimation in Fremyella diplosiphon. Photosynth Res 118:95–104

    Article  CAS  Google Scholar 

  • Singh SP, Ha SY et al (2014) Photoheterotrophic growth unprecedentedly increases the biosynthesis of mycosporine-like amino acid shinorine in the cyanobacterium Anabaena sp. isolated from hot springs of Rajgir (India). Acta Physiol Plant 36:389–397

    Article  CAS  Google Scholar 

  • Singh VK, Jha S et al (2023) Resilience and mitigation strategies of cyanobacteria under ultraviolet radiation stress. Int J Mol Sci 24(15):12381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha RP, Klisch M et al (2001) Responses of aquatic algae and cyanobacteria to solar UV-B. In: Rozema J, Manetas Y, Björn LO (eds) Responses of plants to UV-B radiation. Springer, Dordrecht, pp 219–236

    Chapter  Google Scholar 

  • Sobczyk A, Schyns G et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song JY, Cho HS et al (2011) Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 108(26):10780–10785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stadnichuk IN, Krasilnikov PM (2023) Relationship between non-photochemical quenching efficiency and the energy transfer rate from phycobilisomes to photosystem II. Photosynth Res. https://doi.org/10.1007/s11120-023-01031-z

    Article  PubMed  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69(1):183–215

    Article  CAS  PubMed  Google Scholar 

  • Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63(2):479–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terauchi K, Ohmori M (2004) Blue light stimulates cyanobacterial motility via a cAMP signal transduction system. Mol Microbiol 52:303–309

    Article  CAS  PubMed  Google Scholar 

  • Terauchi K, Montgomery BL et al (2004) RcaE is a complementary chromatic adaptation photoreceptor required for green and red-light responsiveness. Mol Microbiol 51:567–577

    Article  CAS  PubMed  Google Scholar 

  • Villafani Y, Yang HW, Park YI (2020) Color sensing and signal transmission diversity of cyanobacterial phytochromes and cyanobacteriochromes. Mol Cells 43(6):509–516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vogeley L, Sineshchekov OA et al (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0Å. Science 306:1390–1393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner JR, Brunzelle JS et al (2005) A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438:325–331

    Article  CAS  PubMed  Google Scholar 

  • Walters KJ, Whitaker MJ et al (2013) Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon. Commun Integr Biol 6(5):e25005

    Article  Google Scholar 

  • Wang F, Chen M (2022) Chromatic acclimation processes and their relationships with phycobiliprotein complexes. Microorganisms 10(8):1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26(6):369–376

    Article  CAS  PubMed  Google Scholar 

  • Wilde A, Churin Y et al (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett 406:89–92

    Article  CAS  PubMed  Google Scholar 

  • Wiltbank LB, Kehoe DM (2016) Two cyanobacterial photoreceptors regulate photosynthetic light harvesting by sensing teal, green, yellow, and red light. mBio 7:e02130–15

  • Wiltbank LB, Kehoe DM (2019) Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nat Rev Microbiol 17(1):37–50

    Article  CAS  PubMed  Google Scholar 

  • Xue L, Zhang Y et al (2005) Effects of enhanced ultraviolet-B radiation on algae and cyanobacteria. Crit Rev Microbiol 31:79–89

    Article  PubMed  Google Scholar 

  • Yang Y, Lam V et al (2018) Phototaxis in a wild isolate of the cyanobacterium Synechococcus elongatus. Proc Natl Acad Sci USA 115(52):12378–12387

    Article  Google Scholar 

  • Yerrapragada S, Shukla A et al (2015) Extreme sensory complexity encoded in the 10-megabase draft genome sequence of the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601. Genome Announc 3(3):e00355–15

  • Yoshihara S, Ikeuchi M (2004) Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol Sci 3:512–518

    Article  CAS  PubMed  Google Scholar 

  • Yoshihara S, Suzuki F et al (2000) Novel putative photoreceptor and regulatory genes required for the positive phototactic movement of the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 41(12):1299–1304

    Article  CAS  PubMed  Google Scholar 

  • Yoshihara T, Katoh R et al (2004) Identification of reactive species in photoexcited nanocrystalline TiO2 films by wide-wavelength-range (400–2500 nm) transient absorption spectroscopy. J Phys Chem B 108(12):3817–3823

    Article  CAS  Google Scholar 

  • Yoshihara S, Shimada T et al (2006) Reconstitution of blue-green reversible photoconversion of a cyanobacterial photoreceptor, PixJ1, in phycocyanobilin-producing Escherichia coli. Biochemistry 45:3775–3784

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Gan F et al (2015) RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). Front Microbiol 6:1303

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The financial support from the Science and Engineering Research Board (SERB), New Delhi (SCP/2022/000201) is greatly acknowledged. This work is also supported by the funding from Institute of Eminence incentive grant, Banaras Hindu University (R/Dev/D/IOE/Incentive/2021-2022/32399). AG thanks ICMR, New Delhi for the senior research fellowship (3/1/3/JRF-2019/HRD-LS). PP is thankful to the Council of Scientific and Industrial Research (CSIR), New Delhi, India (09/0013(15476)/2022-EMR-I) for the junior research fellowships. RG (NTA Ref. No.-211610075296) and ST (NTA Ref. No.-201610202339) are thankful to the UGC, New Delhi, India for the junior research fellowship. We thank Deepa Pandey for reading this manuscript and for making valuable suggestions.

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  1. Department of Botany, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, UP, 221005, India

    Anjali Gupta, Priyul Pandey, Rinkesh Gupta, Sapna Tiwari & Shailendra Pratap Singh

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  1. Anjali Gupta
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  2. Priyul Pandey
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AG, PP and SPS conceptualized the idea. AG, PP and SPS wrote MS. RG developed figures. ST and SPS edited the MS.

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Correspondence to Shailendra Pratap Singh.

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Gupta, A., Pandey, P., Gupta, R. et al. Responding to light signals: a comprehensive update on photomorphogenesis in cyanobacteria. Physiol Mol Biol Plants 29, 1915–1930 (2023). https://doi.org/10.1007/s12298-023-01386-6

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