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

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 plasticit...

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Published inMolecular 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
LanguageEnglish
Published England Blackwell Publishing Ltd 01.04.2024
Wiley-Blackwell
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Summary: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.
Bibliography:Jake T. Herb, Preeti Bhanap, Katie Lam, and Angie Vreugdenhil equal second author contributions (each contributed a figure).
Rylee K. Hackley and Sungmin Hwang equal first author contributions (each contributed multiple figures, data analysis, project oversight, writing).
Cynthia L. Darnell and Mar Martinez Pastor equal third author contributions (provided mentorship, impactful ideas, experimental design, paper edits).
ObjectType-Article-1
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DE‐FG02‐05ER15650
USDOE
ISSN:0950-382X
1365-2958
DOI:10.1111/mmi.15225