Structure, function, and evolution of microbial phytochromes

Light is the dominant environmental signal for almost all cellular organisms, providing both the energy (either direct or indirect) necessary for growth and metabolism and the sensory information helpful for adaptation. Like plants, microorganisms are profoundly influenced by their surrounding light environment (Hder, 1987; Armitage, 1997; Loros and Dunlap, 2001; Braatsch and Klug, 2004). For photosynthetic species, various photosensory systems provide positional information to optimise light capture and to help minimize damage inflicted by excess solar radiation. In the short term, these sensory systems help these microbes move/grow toward more favourable light fluences. In the long term, they help the organism adjust to the spectral quality of the light (sun versus shade) by modulating the complement of photosynthetic accessory pigments, and/or entrain their growth and development to the diurnal and possibly seasonal cycles. For non-photosynthetic microorganisms, light is also an important environmental cue. Here, light directs preference/avoidance and adaptive strategies similar to those used by photosynthetic species, which in turn enhances their survival or assists them in locating more favourable ecological niches. Whereas the architectures of the microbial photoreceptor systems used for energy capture are known in exquisite detail, we have begun to appreciate only recently the repertoire of photoreceptors employed for sensory information. Much of this new understanding has emerged from the exponentially expanding number of completely sequenced genomes that can now be easily searched for signature photoreceptor motifs by the BLAST algorithm. Recent examples include the discovery of retinal-based bacteriorhodopsin, p-hydroxycinnamic acid-based xantopsin, and flavin-based LOV-type and cryptochrome-type photoreceptors in a variety of bacterial, fungal and animal species (van der Horst and Hellingwerf, 2004; Venter et al., 2004; see Chapters 11, 13). Phytochromes (Phys) are one of the best examples where genome analyses have greatly enhanced our understanding of light perception in the microbial world. This class of photoreceptors is defined by the use of a bilin (or linear tetrapyrrole) chromophore (Smith, 2000; Quail, 2002). Once bound to the apoprotein, the bilin enables detection of red (R) and far-red (FR) light by photointerconversion between two relatively stable conformations, a R-absorbing Pr form and a FR-absorbing Pfr form. Through their unique ability to photointerconvert between Pr and Pfr reversibly, Phys act as light-regulated switches by having one form behave as " active" and the other as " inactive". This photochromicity also can provide a crude form of colour vision through measurement of the Pr/Pfr ratio generated by alterations in the relative amounts of R and FR (Smith, 2000). Phy-type pigments were first discovered over 50 years ago in higher plants based on the ability of R and FR to control many agriculturally important aspects of their life cycle (see Chapters 1, 22; Smith, 2000; Quail, 2002). More recently, genetic analyses and BLAST searches have dramatically expanded their distribution to other kingdoms with the discovery of similar photoreceptors in proteobacteria, cyanobacteria, actinobacteria, filamentous fungi, and possibly slime molds (Wu and Lagarias, 2000; Vierstra, 2002) and B. Karniol and R.D. Vierstra, unpublished). The purpose of this chapter is to review our current understanding of these microbial Phys. As will be seen, they offer simple models to help unravel the biochemical and biophysical events that initiate signal transmission by these novel photochromic pigments. Microbial Phys also provide new clues concerning the evolution of what is now emerging as a superfamily of Phy-type pigments. Their widespread distribution alone implies that light has more important roles in microbial ecology than was previously appreciated, especially for heterotrophic species. Defining these roles will eventually shed new light on the intricate interplay between these species and their surroundings.