Locked Chromophore Analogs Reveal That Photoactive Yellow Protein Regulates Biofilm Formation in the Deep Sea Bacterium <i>Idiomarina loihiensis</i>

<i>Idiomarina loihiensis</i> is a heterotrophic deep sea bacterium with no known photobiology. We show that light suppresses biofilm formation in this organism. The genome of <i>I. loihiensis</i> encodes a single photoreceptor protein: a homologue of photoactive yellow protein (PYP), a blue light receptor with photochemistry based on trans to cis isomerization of its <i>p</i>-coumaric acid (<i>p</i>CA) chromophore. The addition of trans-locked <i>p</i>CA to <i>I. loihiensis</i> increases biofilm formation, whereas cis-locked <i>p</i>CA decreases it. This demonstrates that the PYP homologue regulates biofilm formation in <i>I. loihiensis</i>, revealing an unexpected functional versatility in the PYP family of photoreceptors. These results imply that <i>I. loihiensis</i> thrives not only in the deep sea but also near the water surface and provide an example of genome-based discovery of photophysiological responses. The use of locked <i>p</i>CA analogs is a novel and generally applicable pharmacochemical tool to study the in vivo role of PYPs irrespective of genetic accessibility. Heterologously produced PYP from <i>I. loihiensis</i> (Il PYP) absorbs maximally at 446 nm and has a <i>p</i>CA p<i>K</i><sub>a</sub> of 3.4. Photoexcitation triggers the formation of a pB signaling state that decays with a time constant of 0.3 s. FTIR difference signals at 1726 and 1497 cm<sup>−1</sup> reveal that active-site proton transfer during the photocycle is conserved in Il PYP. It has been proposed that a correlation exists between the lifetime of a photoreceptor signaling state and the time scale of the biological response that it regulates. The data presented here provide an example of a protein with a rapid photocycle that regulates a slow biological response.