David M. Kehoe1 Department of Biology, Indiana University, Bloomington, IN 47405
O
ne of the most fascinating recent developments in the field of microbiology is the growing recognition that a large number of bacterial species are capable of sensing and responding to many different light colors. Much of this has come from analysis of bacterial genome sequences, which has shown that genes encoding a superfamily of phytochrome-class photoreceptors exist in both nonphotosynthetic and photosynthetic prokaryotes (1). Cyanobacteria, which make their living via photosynthesis, contain an especially large number of genes encoding such photoreceptors. As yet, the mechanisms and cellular roles of most of these have not been elucidated. In PNAS, Hirose et al. (2) provide interesting new insights into a cyanobacterial phytochrome-regulated sensory system that controls the production of proteins used to capture light for photosynthesis, raising new possibilities to explain how such systems evolved. Phytochromes, identified in plants more than 50 years ago, have been intensively studied (3). They sense light color using a bilin chromophore and undergo photoreversible conversion between red and farred light-absorbing forms, thereby regulating many aspects of plant growth and development. Despite a growing understanding of their structure and function, plant phytochromes remained orphan photoreceptors for decades. Many suspected that they came from cyanobacteria, and in the 1990s two groups provided the first solid evidence for this. The sequenced genome of Synechocystis PCC 6803 revealed possible phytochrome-encoding genes (4) and complementation of a Fremyella diplosiphon UTEX 481 (Tolypothrix PCC 7601) mutant that had lost its ability to correctly light regulate the production of its photosynthetic light-harvesting proteins uncovered the phytochrome-class photoreceptor RcaE (5, 6). An interesting feature of the cyanobacterial phytochrome family is that, unlike plant phytochromes, many members maximally respond to colors other than red and far red. This was suggested by the discovery of RcaE because it controls a red–green light response, but direct biochemical proof has come from other cyanobacterial phytochrome-class proteins, which show blue–green, green–red, www.pnas.org/cgi/doi/10.1073/pnas.1004510107
Fig. 1. Phycobiliproteins, bilin variation, and group III CA regulation. (A) Phycocyanin and phycoerythrin (blue and red lines, and in vials) absorb in regions of the visible spectrum not well absorbed by chlorophyll or carotenoids. Attached bilins: PEB, phycoerythrobilin; PCB, phycocyanobilin. (B) Natural diversity in coloration of many different cyanobacterial species due to variation in their bilin content [photograph by Christophe Six. Reproduced with permission from Six et al. (2007) (Copyright 2010, Biomed Central Ltd.)]. (C) Group III CA regulation model for F. diplosiphon in red light, showing the asymmetric regulation of red-light active genes (orange) and green-light active genes (yellow) by the Rca and Cgi systems. Dashed line represents proposed repression by the Cgi system; yellow balls, phosphoryl groups; blue boxes, RcaC binding sites.
and violet–yellow photoreversibility (reviewed in ref. 7). Why did cyanobacterial phytochromes evolve to sense such a rainbow of colors? An important reason is that cyanobacteria often live in freshwater or marine environments. Because water preferentially absorbs longer wavelength (more red) light, cells at the surface of a water column experience more red-enriched light than at moderate depth, where green and blue light predominate, or even deeper, where only blue light penetrates. The result is that many cyanobacterial species experience dramatic differences in light-color ratios in their natural environments compared with land plants. At least in part because of this environment, most cyanobacteria use various bilins as the primary pigments in their
photosynthetic light harvesting antennae, or phycobilisomes, which allows photon capture between the blue and red regions of the spectrum that are not efficiently trapped by chlorophyll (Fig. 1A). These bilins can confer dramatic color phenotypes (Fig. 1B). However, because each bilin type absorbs a relatively specific light color, the ability to control the production of a variety of bilin-containing phycobilisomes, each with an absorption profile that closely matches the ambient light color, can Author contributions: D.M.K. wrote the paper. The author declares no conflict of interest. See companion article on page 8854 in issue 19 of volume 107. 1
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PNAS | May 18, 2010 | vol. 107 | no. 20 | 9029–9030
COMMENTARY
Chromatic adaptation and the evolution of light color sensing in cyanobacteria
provide a fitness advantage (8). This process, called “chromatic adaptation” (CA) (9–11) requires cyanobacteria to precisely measure ratios of specific light colors in its environment, a perfect task for phytochrome photoreceptors. CA occurs in lakes and oceans worldwide. Several types of CA have been defined, and all of these exist in species that produce two distinct types of phycobiliproteins, the red-absorbing phycocyanin (PC) and green-absorbing phycoerythrin (PE) (12, 13). More than 70% of the PEcontaining cyanobacteria examined chromatically adapt (12). Because this process dramatically increases the efficiency of photon capture for photosynthesis, and because approximately half of global photosynthesis and oxygenic production has been attributed to phytoplankton (14), of which cyanobacteria are a major part, CA is likely an important contributor to global primary productivity. What occurs during CA? An early study grouped chromatically adapting species based on their PC and PE content during growth in red and green light (12). Group I species have unaltered PC and PE levels during growth in these two light conditions. Group II species have PE levels that are high in green light/low in red light, whereas PC levels are not affected by light color. Group III species are the most complex. They also have PE levels that are high in green light/low in red light, like group II, but in addition, they regulate their PC content in response to light color: PC levels are high in red light and low in green light, just the opposite of the way that PE is regulated. A more recently discovered fourth type (13) is somewhat different from the above processes because the PC and PE do not change; instead, a green-lightabsorbing bilin is added to PE in green light and a blue-light-absorbing bilin is added to PE in blue light (15). What signal transduction pathways control CA and how did they evolve? Studies have focused on the group III species F. diplosiphon because of its dramatic phenotype. This research has revealed that during growth in red light, a complex two-
The simultaneous function of RcaC as an activator and repressor is likely due to the placement and orientation of its DNA binding site. In addition to the Rca system, an additional regulatory pathway called the Cgi (control of green light induction) system controls only green-light-expressed genes involved in PE production. The Cgi system has not yet been characterized. However, its existence prompted the hypothesis that group II chromatic adaptors, with their ability to regulate only greenlight-expressed, PE-producing genes, possess only the Cgi system, and that group III species evolved dual control of red-lightexpressed, PC producing genes and even more regulation of the green-lightexpressed, PE-producing genes through the addition of the Rca system (11). Is this how the signal transduction mechanisms controlling group II and group III CA actually evolved? Hirose et al. provide an intriguing set of data to begin to address this question by showing that a phytochrome-regulated two-component system is responsible for controlling the CA response in the group II chromatic adaptor Nostoc punctiforme. They show that CcaS, which is closely related to RcaE, is the green–red-sensing phytochrome photoreceptor that controls the group II CA response. They also show that the response regulator CcaR, which is
ACKNOWLEDGMENTS. Work on chromatic adaptation in my laboratory was supported by National Science Foundation Grant MCB-0519433.
1. Karniol B, Wagner JR, Walker JM, Vierstra RD (2005) Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem J 392:103–116. 2. Hirose Y, Narikawa R, Katayama M, Ikeuchi M (2010) Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. Proc Natl Acad Sci USA 107: 8854–8859. 3. Kendrick RE, Kronenberg GHM (1994) Photomorphogenesis in Plants (Kluwer, Dordrecht, The Netherlands), 2nd Ed. 4. Kaneko T, et al. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential proteincoding regions. DNA Res 3:109–136.
5. Kehoe DM, Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412. 6. Terauchi K, Montgomery BL, Grossman AR, Lagarias JC, Kehoe DM (2004) RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol Microbiol 51:567–577. 7. Ikeuchi M, Ishizuka T (2008) Cyanobacteriochromes: A new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem Photobiol Sci 7: 1159–1167. 8. Stomp M, et al. (2008) The timescale of phenotypic plasticity and its impact on competition in fluctuating environments. Am Nat 172:E169–E185. 9. Tandeau de Marsac N (2003) Phycobiliproteins and phycobilisomes: The early observations. Photosynth Res 76:197–205.
10. Grossman AR (2003) A molecular understanding of complementary chromatic adaptation. Photosynth Res 76:207–215. 11. Kehoe DM, Gutu A (2006) Responding to color: The regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57:127–150. 12. Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130: 82–91. 13. Palenik B (2001) Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 67: 991–994. 14. Fuhrman J (2003) Genome sequences from the sea. Nature 424:1001–1002. 15. Everroad C, et al. (2006) Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. J Bacteriol 188:3345–3356.
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component signal transduction pathway called the Rca system activates red-lightexpressed genes that produce PC and represses green-light-expressed genes that produce PE. The Rca system operates via the phytochrome-class photoreceptor RcaE, a small-response regulator called RcaF, and the binding of an OmpR-class response regulator called RcaC to the promoters of these genes (Fig. 1C) (11).
CA is likely an important contributor to global primary productivity.
similar to RcaC, is essential for the activation of a green-light-expressed operon in this species, and directly binds to a region of DNA upstream of this operon. Based on the ccaS/ccaR mutant phenotypes, Hirose et al. (2) propose that CcaS autophosphorylation and CcaR binding activity are induced by green light, and that the dephosphorylation of CcaR by CcaS is induced by red light. Intriguingly, such activities are the exact opposite of those proposed for RcaE/RcaC in the group III chromatic adaptor F. diplosiphon, where RcaE appears to phosphorylate (activate) RcaC in red light and dephosphorylate (inactivate) RcaC in green light (11). Although neither model has yet been biochemically proven, all available genetic and molecular data strongly suggest that both are accurate. These data may provide a straightforward way to explain the evolution of the regulation of group III CA: a two-component system regulated by a red–green phytochrome photoreceptor (such as the CcaS/CcaR system) was duplicated and diverged to respond to red and green light in a manner directly opposite to that of its ancestor. The next important question is: does the Cgi system of a group III CA species such as F. diplosiphon consist of a transcriptional control pathway that is made up of CcaS and CcaR homologs, or has nature evolved something more complex than this? Because the F. diplosiphon genome is not yet available for the kind of genome sequence analysis that led to the discovery of CcaS and CcaR in N. punctiforme, this question remains unanswered for the moment. But given the fact that cyanobacteria have been evolving since the Precambrian era, and considering the twists and turns that have accompanied the unraveling of the chromatic adaptation regulatory pathways in F. diplosiphon over the past few decades, we may still be in for several more surprises before the story of the evolution of these color-sensing systems is completely told.
Kehoe
