Integration of Temperature and Blue‐Light Sensing in Acinetobacter baumannii Through the BlsA Sensor

Abstract

BlsA is a BLUF photoreceptor present in Acinetobacter baumannii, responsible for modulation of motility, biofilm formation and virulence by light. In this work, we have combined physiological and biophysical evidences to begin to understand the basis of the differential photoregulation observed as a function of temperature. Indeed, we show that blsA expression is reduced at 37°C, which correlates with negligible photoreceptor levels in the cells, likely accounting for absence of photoregulation at this temperature. Another point of control occurs on the functionality of the BlsA photocycle itself at different temperatures, which occurs with an average quantum yield of photoactivation of the signaling state of 0.20 ± 0.03 at 15°C < T < 25°C, but is practically inoperative at T > 30°C, as a result of conformational changes produced in the nanocavity of FAD. This effect would be important when the photoreceptor is already present in the cell to avoid almost instantaneously further signaling process when it is no longer necessary, for example under circumstances of temperature changes possibly faced by the bacteria. This complex interplay between light and temperature would provide the bacteria clues of environmental location and dictate/modulate light photosensing in A. baumannii.

A Light-Regulated Type I Pilus Contributes to Acinetobacter baumannii Biofilm, Motility, and Virulence Functions

“…This response could be attributed to the significantly reduced constitutive transcription of blsA in cells cultured at this temperature (24). The negative effect of a temperature of 37°C on blsA transcription was recently confirmed by work reported by Abatedaga et al (27), which also showed the predicted reduction in BlsA production as well as the observation that temperatures higher than 30°C significantly impair the photocycle of purified BlsA protein. Thus, the ability of the 17978 parental strain incubated at 37°C to produce comparable surface motility responses in the presence and absence of light under the conditions described in this report (Fig.…”

“…In this report, we show that the light-regulated motility and biofilm and pellicle formation responses displayed by A. baumannii ATCC 17978 (17978) depend on the active expression of the photoregulated pilus assembly system PrpABCD in a BlsAmediated process when bacteria are cultured at 24°C. PrpABCD also proved to be critical for the interaction of polarized A549 human alveolar epithelial cells with 17978 and the virulence of this strain to Galleria mellonella when tested at 37°C, a temperature at which BlsA-mediated light regulation is lost because of a drastic reduction in blsA expression and an alteration of the BlsA reversible photocycle at temperatures higher than 30°C (24,27). However, the ability of a 17978 prpA mutant to display lightregulated surface motility and biofilm responses at 37°C indicates that undetermined additional 17978 factors involved in these responses are controlled by light in a BlsA-independent regulatory process that remains to be identified and characterized.…”

Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans

“…We interpret the spectral changes of FphA with rising temperatures, leading to spectra which resemble the free chromophore, as resulting from a ‘softening’ of the chromophore pocket. Similarly, temperature dependence of UV/Vis spectra of the BLUF protein BlsA from Acinetobacter baumannii was attributed to a loss of rigidity of the FAD‐binding pocket with increasing temperatures (Abatedaga et al , ). The temperature‐induced changes of spectral properties were not reversible for full‐length FphA.…”

“…Given that there is some biochemical evidence that the phytochrome from the aquatic (marine and freshwater) cyanobacterium Synechocystis PCC6803, Cph1, also acts as temperature sensor (Njimona et al , ), we are tempted to speculate that temperature sensing could be the ancient function of phytochromes that was already present before the photoreceptor function of this family of proteins evolved. There is evidence that blue‐light receptors such as phototropin or BLUF photoreceptors also respond to temperature (Abatedaga et al , ; Fujii et al , ).…”

Molecular characterization of DXCF cyanobacteriochromes from the cyanobacterium Acaryochloris marina identifies a blue-light power sensor

“…A dark-reversion property generally enables photoreceptors to sense light intensity signals in a temperature-dependent manner. In fact, other photoreceptors belonging to different families such as phytochrome, light, oxygen, or voltage (LOV) and blue-light using flavin (BLUF) proteins have also been revealed to show similar behaviors (41)(42)(43)(44)(45). In the case of the phytochrome proteins, Cph1 and Agp1 showed unexpected temperature-dependent His kinase activities, which affected conjugation in Agrobacterium.…”