TbsP and TrmB jointly regulate gapII to influence cell development phenotypes in the archaeon Haloferax volcanii

• Published in: Molecular microbiology Vol. 121; no. 4; pp. 742 - 766
• Main Authors: Hackley, Rylee K., Hwang, Sungmin, Herb, Jake T., Bhanap, Preeti, Lam, Katie, Vreugdenhil, Angie, Darnell, Cynthia L., Pastor, Mar Martinez, Martin, Johnathan H., Maupin‐Furlow, Julie A., Schmid, Amy K.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.04.2024; Wiley-Blackwell
• Subjects: Archaea; Biofilms; Biogenesis; Cell density; Cell morphology; Cell surface; central metabolism; Cytology; Environmental changes; Environmental conditions; Enzymes; Evolution; Gene expression; gene regulatory network; Genetic suppression; Genetics; Gluconeogenesis; Glucose; Glycoproteins; Haloferax volcanii; Metabolic pathways; Microorganisms; Morphology; Motility; Nutrients; Phenotypes; Phenotyping; Salinity; Transcription; transcription factor; transcription factor; Haloferax volcanii; Archaea; central metabolism; cell morphology; gene regulatory network; gluconeogenesis
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.15225

Microbial cells must continually adapt their physiology in the face of changing environmental conditions. Archaea living in extreme conditions, such as saturated salinity, represent important examples of such resilience. The model salt‐loving organism Haloferax volcanii exhibits remarkable plasticity in its morphology, biofilm formation, and motility in response to variations in nutrients and cell density. However, the mechanisms regulating these lifestyle transitions remain unclear. In prior research, we showed that the transcriptional regulator, TrmB, maintains the rod shape in the related species Halobacterium salinarum by activating the expression of enzyme‐coding genes in the gluconeogenesis metabolic pathway. In Hbt. salinarum, TrmB‐dependent production of glucose moieties is required for cell surface glycoprotein biogenesis. Here, we use a combination of genetics and quantitative phenotyping assays to demonstrate that TrmB is essential for growth under gluconeogenic conditions in Hfx. volcanii. The ∆trmB strain rapidly accumulated suppressor mutations in a gene encoding a novel transcriptional regulator, which we name trmB suppressor, or TbsP (a.k.a. “tablespoon”). TbsP is required for adhesion to abiotic surfaces (i.e., biofilm formation) and maintains wild‐type cell morphology and motility. We use functional genomics and promoter fusion assays to characterize the regulons controlled by each of TrmB and TbsP, including joint regulation of the glucose‐dependent transcription of gapII, which encodes an important gluconeogenic enzyme. We conclude that TrmB and TbsP coregulate gluconeogenesis, with downstream impacts on lifestyle transitions in response to nutrients in Hfx. volcanii. The transcription factors TrmB and TbsP coregulate the gluconeogenic enzyme‐coding gene gapII to influence cell lifestyle transitions in hypersaline archaea. The proposed model of regulation is shown above, and the motile‐to‐sessile transition that is indirectly influenced by this regulation is shown below.