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Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors

Abstract

Cyanobacteria are an evolutionarily and ecologically important group of prokaryotes. They exist in diverse habitats, ranging from hot springs and deserts to glaciers and the open ocean. The range of environments that they inhabit can be attributed in part to their ability to sense and respond to changing environmental conditions. As photosynthetic organisms, one of the most crucial parameters for cyanobacteria to monitor is light. Cyanobacteria can sense various wavelengths of light and many possess a range of bilin-binding photoreceptors belonging to the phytochrome superfamily. Vital cellular processes including growth, phototaxis, cell aggregation and photosynthesis are tuned to environmental light conditions by these photoreceptors. In this Review, we examine the physiological responses that are controlled by members of this diverse family of photoreceptors and discuss the signal transduction pathways through which these photoreceptors operate. We highlight specific examples where the activities of multiple photoreceptors function together to fine-tune light responses. We also discuss the potential application of these photosensing systems in optogenetics and synthetic biology.

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Fig. 1: Behaviour of a cyanobacterial phytochrome superfamily photoreceptor dimer in response to changes in ambient light colour.
Fig. 2: Domains of cyanobacterial phytochrome superfamily members with a known physiological role.
Fig. 3: Common physiological responses controlled by cyanobacterial phytochrome superfamily photoreceptors.
Fig. 4: Complex interactions between cyanobacteriochromes and downstream signal transduction during type III chromatic acclimation in the aquatic cyanobacterium Fremyella diplosiphon Fd33.
Fig. 5: Coordination of cell aggregation by a network of cyanobacteriochromes in Thermosynechococcus vulcanus RKN.

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Acknowledgements

The authors thank the referees of this Review for their substantial efforts to help improve the manuscript. They also thank J. Sanfilippo and other members of the Kehoe laboratory, as well as M. Wiltbank, for their valuable thoughts and insights. This work was supported by the Office of the Vice Provost for Research at Indiana University, Bloomington, through its Bridge Funding Program to D.M.K. and by a National Science Foundation Grant to D.M.K. (MCB-1818187).

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Nature Reviews Microbiology thanks A. Wilde and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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D.M.K. and L.B.W. researched the data for the article, substantially contributed to discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to David M. Kehoe.

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Glossary

Irradiance

The amount of radiant energy received by a surface per unit time and unit area.

Photoautotrophic

The ability to use light to produce food from inorganic molecules.

Chromophore

A small molecule or region that imparts light sensing to a protein.

Bilins

Pigments produced from porphyrins that can function as chromophores for photoreceptors and photosynthetic light-harvesting proteins.

Photocycle

The series of structural changes that a photoreceptor undergoes upon light absorption before returning to its initial structure.

Optogenetics

The biological engineering of specific cellular processes in living cells to be controlled by light.

Photosensory module

A collection of domains within a photoreceptor that binds a bilin chromophore and endows the ability to sense and respond to light.

PAS domain

A widespread protein structural domain that is commonly involved in protein–protein interactions or functions as a sensor in signal transduction pathways. PAS is an abbreviation of Per-Arnt-Sim, the proteins in which this domain was first discovered.

GAF domain

A domain that is widely found in eukaryotes and prokaryotes and is structurally similar to a PAS domain. Among its many roles, it binds chromophores and functions as a photoreceptor. GAF is an abbreviation of cGMP phosphodiesterases, adenylyl cyclases and FhiA, the names of three proteins that contain this domain.

PHY domain

A domain that is structurally related to a GAF domain and is found specifically in the photosensory module of phytochromes and stabilizes the light-activated state. PHY is an abbreviation for phytochrome-specific protein.

Output domain

A domain of a signal transduction protein with the capacity to elicit a molecular or cellular response. In photoreceptors, its function may be modulated by the photosensory module.

MCP domain

A membrane-spanning sensory molecule in bacteria first identified as a chemical sensor that transmits its signal through a two-component system histidine–aspartate phosphotransfer reaction. MCP is an acronym for methyl-accepting chemotaxis protein.

GGDEF domain

A domain that is present in many bacterial proteins and synthesizes the second messenger cyclic diguanosine monophosphate (c-di-GMP), typically under the regulation of another domain. GGDEF is an abbreviation of a five amino acid motif (Gly–Gly–Asp–Glu–Phe) in the domain.

EAL domain

A domain that is responsible for hydrolysis of the second messenger cyclic diguanosine monophosphate (c-di-GMP). EAL is based on the highly conserved sequence motif (Glu–Ala–Leu) near the amino-terminal end of the domain.

Phycobilisomes

Light-harvesting antennae of some photosynthetic organisms. These are water soluble, located on the surface of photosynthetic membranes and composed of pigmented and non-pigmented proteins. In cyanobacteria, they are typically hemidiscoidal structures with rods radiating from an inner core.

Absorbance maximum

max). The wavelength that is maximally absorbed by the chromophore or light-absorbing protein being examined.

Cgi system

A post-transcriptional regulatory pathway that modulates light-responsive gene expression during chromatic acclimation in the cyanobacterium Fremyella diplosiphon Fd33 Cgi is an acronym for control of green light induction.

Morphogenes

Genes whose protein product causes a change in cell morphology.

Photorespiration

A metabolic process in photosynthetic organisms that causes the oxygenation of ribulose-1,5-bisphosphate, reducing the amount of 3-phosphoglycerate produced during the Calvin–Benson cycle and wasting energy obtained by the light-dependent reactions of photosynthesis.

Carboxysome

A bacterial compartment, made of proteins and containing the enzymes ribulose-1,5-bisphosphate carboxylase/oxygenase and carbonic anhydrase, where carbon dioxide is concentrated to increase the efficiency of carbon fixation during photosynthesis.

Allophycocyanin

One of the bilin-containing proteins, or phycobiliproteins, typically found in the central or core region of photosynthetic light-harvesting antennae called phycobilisomes.

Cyclic diguanosine monophosphate

(c-di-GMP). A widespread second messenger in bacterial cells that controls cell movement and many developmental processes.

Twitching motility

A type of motility carried out by bacteria on solid surfaces using hair-like filaments called type IV pili.

PATAN domain

A domain within a response regulator involved in cyanobacterial heterocyst patterning during nitrogen starvation. The PATAN domain is found in many prokaryotes and regulates motility and development through protein–protein interactions. PATAN is an abbreviation of PatA amino terminus.

PilZ domain

Named after the type IV pilus control protein PilZ, these domains are capable of binding cyclic diguanosine monophosphate (c-di-GMP), which causes a conformation change and leads to physiological responses including a shift from a motile to sessile state.

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Wiltbank, L.B., Kehoe, D.M. Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nat Rev Microbiol 17, 37–50 (2019). https://doi.org/10.1038/s41579-018-0110-4

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