From Plant Infectivity to Growth Patterns: The Role of Blue-Light Sensing in the Prokaryotic World

Review From Plant Infectivity to Growth Patterns: The Role of Blue-Light Sensing in the Prokaryotic World

Abstract: Flavin-based photoreceptor proteins of the LOV (Light, Oxygen, and Voltage) and BLUF (Blue Light sensing Using Flavins) superfamilies are ubiquitous among the three life domains and are essential blue-light sensing systems, not only in plants and algae, but also in prokaryotes. Here we review their biological roles in the prokaryotic world and their evolution pathways. An unexpected large number of bacterial species possess flavin-based photosensors, amongst which are important human and plant pathogens. Still, few cases are reported where the activity of blue-light sensors could be correlated to infectivity and/or has been shown to be involved in the activation of specific genes, resulting in selective growth patterns. Metagenomics and bio-informatic analysis have only recently been initiated, but signatures are beginning to emerge that allow definition of a bona fide LOV or BLUF domain, aiming at better selection criteria for novel blue-light sensors. We also present here, for the first time, the phylogenetic tree for archaeal LOV domains that have reached a statistically significant number but have not at all been investigated thus far.

One. Introduction

A blue-light sensing, flavin-binding receptor (Fl-Blue) that regulates growth patterns and biofilm formation in Listeria monocytogenes, a single, two-cofactor Fl-Blue that integrates blue-light sensing with the detection of the cellular redox state in the facultative phototroph Rhodobacter sphaeroides, a third Fl-Blue that forms a signaling network with a phytochrome-related protein in regulating swarming motility of Pseudomonas syringae, and last, but not least, multiple Fl-Blue that show additive effects during light-induced inhibition of twitching motility in Acinetobacter baylyi: these are only few examples of recent research achievements in the growing field of bacterial flavin-based photosensing, a research area, which emerged during the last decade and is rapidly changing our understanding of how prokaryotes exploit blue-light as a source of information. Most importantly, we are beginning to realize that bacterial blue-light perception integrates with other environmental cues and metabolic signals, e.g., temperature, redox state, and salt stress.

Fl-Blues are becoming increasingly interesting proteins for a number of issues. Their activation and signaling mechanisms, based on non-isomerizable chromophores, have established novel paradigms in photosensory biology and photobiophysics. The biological functions of Fl-Blues have been and are still well-documented in plants, however, are now mirrored by a growing, albeit still limited, understanding of their functional roles in bacteria. The widespread occurrence of Fl-Blues offers a unique possibility of exploring the evolution and ecological significance of blue-light through soluble photoreceptors. Last, but not least, Fl-Blues have a large potential as tools for light-control of cellular functions (optogenetics), and as fluorescent reporters in conditions not suitable for green-fluorescent proteins and derivatives, e.g., anaerobic/microaerobic systems or small viral genomes.

Fl-Blues can be classified as three distinct types: Light-Oxygen-Voltage (LOV), Blue-Light-sensing Using Flavin (BLUF), and cryptochrome (Cry). LOV and BLUF domains are relatively small and compact folds (approximately one hundred to one hundred ten amino acids), binding a single flavin chromophore (FMN, flavin mononucleotide, or FAD, flavin adenine dinucleotide). Their photosensing and photoresponding properties, characterized by defined photochemical reactions and spectral features (vide infra) are linked to diverse effector/regulator functions in a large array of different proteins. Cry, instead are two-chromophore proteins, structurally and functionally related to the DNA-repairing enzymes photolyases, with which they form the large Cry/PL family. Contrary to photolyases, which catalyze the light-dependent repair of UV-induced DNA lesions, Cry proteins mainly function as sensors and have lost or show a strongly reduced capability of DNA repair activity. The divergent Cry/PL superfamily, spread with diverse functional significance in Archaea, Bacteria, and Eukarya (including animals), is still a matter of debate as for the distinction between sensorial and photo-activated photolyase-like activity and will not be dealt further here. The reader is referred to recent manuscripts dealing with key questions, such as: (a) the still controversially discussed photoactivation mechanisms of Cry proteins, relying on antenna chromophores and flavin-centered photoinduced electron transfer reactions; (b) the role of light-activation (e.g., in bacteria, plants, invertebrates) versus light-independent functions in vivo (e.g., in humans); and (c) the long-lasting question of Cry involvement in photo-magnetoreception in migratory birds, via the formation of spin-correlated radical pairs upon blue light excitation.

Here, we will focus on LOV and BLUF proteins, given their peculiar relevance and versatility in the prokaryotic world and their link to their plants counterparts. The manuscript is structured as follows: a brief summary of photoactivation and light-to-signal propagation mechanisms, followed by a comprehensive update on known biological functions of LOV and BLUF proteins in bacteria. We will conclude providing novel results of our most recent survey of databases for prokaryotic LOV and BLUF domains, presenting and applying novel search criteria based on sequence patterns. This genome-mining has brought forth LOV proteins widely present in Archaea, for which we will provide for the first time a phylogenetic, distance-tree analysis of LOV domains.