A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer

Marianne Jaubert,Jérôme Lavergne,Joël Fardoux,Laure Hannibal,Laurie Vuillet,Jean-Marc Adriano,Pierre Bouyer,David Pignol,Eric Giraud,André Verméglio

doi:10.1074/jbc.m611173200

Abstract

Bacteriophytochromes are phytochrome-like proteins that mediate photosensory responses in various bacteria according to their light environment. The genome of the photosynthetic and plant-symbiotic Bradyrhizobium sp. strain ORS278 revealed the presence of a genomic island acquired by lateral transfer harboring a bacteriophytochrome gene, BrBphP3.ORS278, and genes involved in the synthesis of phycocyanobilin and gas vesicles. The corresponding protein BrBphP3.ORS278 is phylogenetically distant from the other (bacterio)phytochromes described thus far and displays a series of unusual properties. It binds phycocyanobilin as a chromophore, a unique feature for a bacteriophytochrome. Moreover, its C-terminal region is short and displays no homology with any known functional domain. Its dark-adapted state absorbs maximally around 610 nm, an unusually short wavelength for (bacterio)phytochromes. This form is designated as Po for orange-absorbing form. Upon illumination, a photo-reversible switch occurs between the Po form and a red (670 nm)-absorbing form (Pr), which rapidly backreacts in the dark. Because of this instability, illumination results in a mixture of the Po and Pr states in proportions that depend on the intensity. These uncommon features suggest that BrBphP3.ORS278 could be fitted to measure light intensity rather than color.

Highlights

To adapt their growth and development to light environment, plants use a large panel of photoreceptors
The architecture of most phytochromes is composed of a N-terminal photosensory core domain (PCD) and of a C-terminal module involved in signal transduction
All bilins are derived from a heme molecule, converted to biliverdin IX (BV) by a heme oxygenase

Summary

The abbreviations used are

Plant phytochrome; BphP, bacteriophytochrome; BV, biliverdin; Cph, cyanobacteria phytochrome; Fph, fungi phytochrome; PCB, phycocyanobilin; PCD, photosensory core domain. A Singular Bacteriophytochrome gen-fixing nodules on both roots and stems of some aquatic legumes belonging to the genus Aeschynomene [18] Besides their life in association with plant, these bacteria develop freely in aquatic environments or in soils. The recent sequencing of the genomes of two photosynthetic Bradyrhizobium strains (ORS278 and BTAi1) revealed the presence of two other BphPs in each strain.. The recent sequencing of the genomes of two photosynthetic Bradyrhizobium strains (ORS278 and BTAi1) revealed the presence of two other BphPs in each strain.5 One of these is common to both strains, whereas the second is specific to each strain. We give evidence that its gene was acquired by lateral gene transfer together with bphO and pcyA genes, involved in its chromophore synthesis This is the first description of a BphP containing phycocyanobilin as chromophore. We show that this new type of BphP possesses a series of unusual photochemical properties, which leads us to propose that it acts as a sensor of light intensity rather than light color

EXPERIMENTAL PROCEDURES

RESULTS

DISCUSSION