Regulation of the Erythrobacter litoralis DSM 8509 general stress response by visible light

Abstract

Extracytoplasmic function (ECF) sigma factors are environmentally responsive transcriptional regulators. In Alphaproteobacteria, σ EcfG activates general stress response (GSR) transcription and protects cells from multiple stressors. A phosphorylation-dependent protein partner switching mechanism, involving HWE/HisKA_2-family histidine kinases, underlies σ EcfG activation. The identity of these sensor kinases and the signals that regulate them remain largely uncharacterized. We have developed the aerobic anoxygenic photoheterotroph (AAP), Erythrobacter litoralis DSM 8509, as a comparative genetic model to investigate GSR. Using this system, we sought to define the role of visible light and a photosensory HWE kinase, LovK, in regulation of GSR transcription. We identified three HWE kinase genes that collectively control GSR: gsrK and lovK are activators, while gsrP is a repressor. In wild-type cells, GSR transcription is activated in the dark and nearly off in the light, and the opposing activities of gsrK and gsrP are sufficient to modulate GSR transcription in response to illumination. In the absence of gsrK and gsrP, lovK alone is sufficient to activate GSR transcription. lovK is a more robust activator in the dark, and light-dependent regulation by LovK requires that its N-terminal LOV domain be photochemically active. Our studies establish a role for visible light and an ensemble of HWE kinases in light-dependent regulation of GSR transcription in E. litoralis.

Dimer Asymmetry and Light Activation Mechanism in Brucella Blue-Light Sensor Histidine Kinase

“…The light dependent virulence enhancement in B. abortus has been linked to upregulation of the LOV-HK activity (3,4). LOV-HK is thought to play an important role in modulating the bacteriumhost interactions in both plants and animals (5)(6)(7)(8)(9)(10)(11)(12) via the response regulator PhyR, a key element of the general stress response in proteobacteria (13)(14)(15)(16)(17). B. abortus LOV-HK comprises an N-terminal blue light-sensing LOV domain, a central PAS (Per-Arnt-Sim) domain of unknown function and a C-terminal HK domain (Fig.…”

Shining light on the alphaproteobacterial general stress response

“…Addition of a new, phototropic lab strain allows for more precise dissection of the GSR network and its interactions with phototrophic genes. Even strains as closely related as E. litoralis HTCC2594 and E. litoralis DSM 8509 show surprising differences; for instance, the GSR is turned on in the dark in DSM 8509 (Fiebig et al , ), while it appears to be activated by light in HTCC2594 (Swartz et al , ; Corrêa et al , ). This difference may be due to the lack of phototrophic genes in HTCC2594 and bears further study, which is now possible due to the efforts of Fiebig and co‐workers.…”

“…The inactive state structure of EL346, along with the crystal structure of the kinase domain of B. abortus LOV‐HK, are the only structural information on HWE/HisKA_2 HKs that we are aware of at this time (Rivera‐Cancel et al , ; Rinaldi et al , ; Herrou et al , ). Interestingly, and as noted by Fiebig et al ., there is a large difference of ~ 150 kb in the genomes of E. litoralis HTCC2594 and E. litoralis DSM 8509, with the former missing many phototrophy genes but also encoding several more LOV domain photosensors (Fiebig et al , ). This difference may be related to the source from which the strains have been isolated (supralittoral zone for DSM 8509 vs 10 m depth for HTCC2594) and the resulting difference in light exposure.…”

“…Many bacteria use a common set of cellular responses, termed the general stress response (GSR), to react to these various conditions encountered throughout their life cycle, including during infection of pathogenic species such as Brucella abortus (Staroń and Mascher, ; Kim et al , ). In this article of Molecular Microbiology , Fiebig et al , report two key uses of the marine alphaproteobacterium Erythrobacter litoralis DSM 8509 to understand the GSR by both (1) developing this organism as a tractable genetic model and (2) using it to demonstrate how a complex network regulates the GSR in response to light/dark changes, both directly and indirectly (Fiebig et al , ). Both sets of findings open up new avenues in bacterial signaling and stress response for researchers to explore.…”

Specific proteomic adaptation to distinct environments in Vibrio parahaemolyticus includes significant fluctuations in expression of essential proteins

“…Moreover, two ferric siderophore receptors revealed a modest, but significant, increase in expression in the cells from the centre during the swarm colony development, namely the ferric vibrioferrin receptor (VPA1656) and the ferric siderophore receptor-like protein (VPA1657) (Supporting Information Table S5). Specialized sigma factors that lead to general stress or heat resistance of cells, such as RpoS and RpoH, respectively, were highly induced in cells from the centre (Cochran et al, 2000;Mandel and Silhavy, 2005;Ait-Ouazzou et al, 2012;Fiebig et al, 2019) (Supporting Information Table S5). Furthermore, oxidative stress response proteins including superoxide dismutase, dehydrogenases and oxidase oxireductases are all components that were upregulated exclusively in the centre of swarm colonies (Supporting Information Table S5).…”