Light-Triggered Carotenogenesis in Myxococcus xanthus: New Paradigms in Photosensory Signaling, Transduction and Gene Regulation.

S Padmanabhan,Elena Pajares-Martínez,Eva Bastida-Martínez,Marta Fontes,Ricardo Pérez-Castaño,Montserrat Elías-Arnanz,Antonio A Iniesta,María Luisa Galbis-Martínez,Diego Bernal-Bernal,María Carmen Polanco,Antonio J Monera-Girona

doi:10.3390/microorganisms9051067

Abstract

Myxobacteria are Gram-negative δ-proteobacteria found predominantly in terrestrial habitats and often brightly colored due to the biosynthesis of carotenoids. Carotenoids are lipophilic isoprenoid pigments that protect cells from damage and death by quenching highly reactive and toxic oxidative species, like singlet oxygen, generated upon growth under light. The model myxobacterium Myxococcus xanthus turns from yellow in the dark to red upon exposure to light because of the photoinduction of carotenoid biosynthesis. How light is sensed and transduced to bring about regulated carotenogenesis in order to combat photooxidative stress has been extensively investigated in M. xanthus using genetic, biochemical and high-resolution structural methods. These studies have unearthed new paradigms in bacterial light sensing, signal transduction and gene regulation, and have led to the discovery of prototypical members of widely distributed protein families with novel functions. Major advances have been made over the last decade in elucidating the molecular mechanisms underlying the light-dependent signaling and regulation of the transcriptional response leading to carotenogenesis in M. xanthus. This review aims to provide an up-to-date overview of these findings and their significance.

Highlights

Light is an important and ubiquitous signal in terrestrial and aquatic ecosystems, and the ability to sense, respond and adapt to light is crucial for most living organisms, including bacteria
Given that carotenoids are in the frontline of the defense against photooxidative stress, light and oxygen-related species like 1 O2 are among the principal environmental factors involved in signaling and triggering carotenoid biosynthesis
Our present review aims to provide a timely update of these findings, from signal reception and transduction to the transcriptional regulation underlying the photooxidative stress response and carotenoid biosynthesis in M. xanthus, and to discuss their mechanistic and evolutionary significance

Summary

Introduction

Light is an important and ubiquitous signal in terrestrial and aquatic ecosystems, and the ability to sense, respond and adapt to light is crucial for most living organisms, including bacteria. Given that carotenoids are in the frontline of the defense against photooxidative stress, light and oxygen-related species like 1 O2 are among the principal environmental factors involved in signaling and triggering carotenoid biosynthesis. This has been amply demonstrated in several studies from plants [15,16] and fungi [17,18] to bacteria [4,8,9,12]. Our present review aims to provide a timely update of these findings, from signal reception and transduction to the transcriptional regulation underlying the photooxidative stress response and carotenoid biosynthesis in M. xanthus, and to discuss their mechanistic and evolutionary significance

Biosynthesis of Carotenoids

CarH and Vitamin B12 Regulate Light-Induced Expression of Carotenoid Genes

Light sensing

Light-Induced Expression of the carQRS Operon and Gene crtIb

Regulation of CarQ Activity in Light-Induced Expression of carQRS and crtIb

Derepression of PB by Light-Induced Expression of the CarS Antirepressor