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Title: GlpR Is a Direct Transcriptional Repressor of Fructose Metabolic Genes in Haloferax volcanii

Abstract

ABSTRACT DeoR-type helix-turn-helix (HTH) domain proteins are transcriptional regulators of sugar and nucleoside metabolism in diverse bacteria and also occur in select archaea. In the model archaeonHaloferax volcanii, previous work implicated GlpR, a DeoR-type transcriptional regulator, in the transcriptional repression ofglpRand the gene encoding the fructose-specific phosphofructokinase (pfkB) during growth on glycerol. However, the global regulon governed by GlpR remained unclear. Here, we compared transcriptomes of wild-type and ΔglpRmutant strains grown on glycerol and glucose to detect significant transcript level differences for nearly 50 new genes regulated by GlpR. By coupling computational prediction of GlpR binding sequences within vivoandin vitroDNA binding experiments, we determined that GlpR directly controls genes encoding enzymes involved in fructose degradation, including fructose bisphosphate aldolase, a central control point in glycolysis. GlpR also directly controls other transcription factors. In contrast, other metabolic pathways appear to be under the indirect influence of GlpR.In vitroexperiments demonstrated that GlpR purifies to function as a tetramer that binds the effector molecule fructose-1-phosphate (F1P). These results suggest thatH. volcaniiGlpR functions as a direct negative regulator of fructose degradation during growth on carbon sources other than fructose, such as glucose and glycerol, and that GlpR bears striking functional similarity to bacterial DeoR-typemore » regulators. IMPORTANCEMany archaea are extremophiles, able to thrive in habitats of extreme salinity, pH and temperature. These biological properties are ideal for applications in biotechnology. However, limited knowledge of archaeal metabolism is a bottleneck that prevents the broad use of archaea as microbial factories for industrial products. Here, we characterize how sugar uptake and use are regulated in a species that lives in high salinity. We demonstrate that a key sugar regulatory protein in this archaeal species functions using molecular mechanisms conserved with distantly related bacterial species.« less

Authors:
; ; ; ; ; ; ; ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Univ. of Florida, Gainesville, FL (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1541706
DOE Contract Number:  
FG02-05ER15650
Resource Type:
Journal Article
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 200; Journal Issue: 17; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
Microbiology

Citation Formats

Martin, Jonathan H., Sherwood Rawls, Katherine, Chan, Jou Chin, Hwang, Sungmin, Martinez-Pastor, Mar, McMillan, Lana J., Prunetti, Laurence, Schmid, Amy K., Maupin-Furlow, Julie A., and Metcalf, William W. GlpR Is a Direct Transcriptional Repressor of Fructose Metabolic Genes in Haloferax volcanii. United States: N. p., 2018. Web. doi:10.1128/jb.00244-18.
Martin, Jonathan H., Sherwood Rawls, Katherine, Chan, Jou Chin, Hwang, Sungmin, Martinez-Pastor, Mar, McMillan, Lana J., Prunetti, Laurence, Schmid, Amy K., Maupin-Furlow, Julie A., & Metcalf, William W. GlpR Is a Direct Transcriptional Repressor of Fructose Metabolic Genes in Haloferax volcanii. United States. doi:10.1128/jb.00244-18.
Martin, Jonathan H., Sherwood Rawls, Katherine, Chan, Jou Chin, Hwang, Sungmin, Martinez-Pastor, Mar, McMillan, Lana J., Prunetti, Laurence, Schmid, Amy K., Maupin-Furlow, Julie A., and Metcalf, William W. Mon . "GlpR Is a Direct Transcriptional Repressor of Fructose Metabolic Genes in Haloferax volcanii". United States. doi:10.1128/jb.00244-18.
@article{osti_1541706,
title = {GlpR Is a Direct Transcriptional Repressor of Fructose Metabolic Genes in Haloferax volcanii},
author = {Martin, Jonathan H. and Sherwood Rawls, Katherine and Chan, Jou Chin and Hwang, Sungmin and Martinez-Pastor, Mar and McMillan, Lana J. and Prunetti, Laurence and Schmid, Amy K. and Maupin-Furlow, Julie A. and Metcalf, William W.},
abstractNote = {ABSTRACT DeoR-type helix-turn-helix (HTH) domain proteins are transcriptional regulators of sugar and nucleoside metabolism in diverse bacteria and also occur in select archaea. In the model archaeonHaloferax volcanii, previous work implicated GlpR, a DeoR-type transcriptional regulator, in the transcriptional repression ofglpRand the gene encoding the fructose-specific phosphofructokinase (pfkB) during growth on glycerol. However, the global regulon governed by GlpR remained unclear. Here, we compared transcriptomes of wild-type and ΔglpRmutant strains grown on glycerol and glucose to detect significant transcript level differences for nearly 50 new genes regulated by GlpR. By coupling computational prediction of GlpR binding sequences within vivoandin vitroDNA binding experiments, we determined that GlpR directly controls genes encoding enzymes involved in fructose degradation, including fructose bisphosphate aldolase, a central control point in glycolysis. GlpR also directly controls other transcription factors. In contrast, other metabolic pathways appear to be under the indirect influence of GlpR.In vitroexperiments demonstrated that GlpR purifies to function as a tetramer that binds the effector molecule fructose-1-phosphate (F1P). These results suggest thatH. volcaniiGlpR functions as a direct negative regulator of fructose degradation during growth on carbon sources other than fructose, such as glucose and glycerol, and that GlpR bears striking functional similarity to bacterial DeoR-type regulators. IMPORTANCEMany archaea are extremophiles, able to thrive in habitats of extreme salinity, pH and temperature. These biological properties are ideal for applications in biotechnology. However, limited knowledge of archaeal metabolism is a bottleneck that prevents the broad use of archaea as microbial factories for industrial products. Here, we characterize how sugar uptake and use are regulated in a species that lives in high salinity. We demonstrate that a key sugar regulatory protein in this archaeal species functions using molecular mechanisms conserved with distantly related bacterial species.},
doi = {10.1128/jb.00244-18},
journal = {Journal of Bacteriology},
issn = {0021-9193},
number = 17,
volume = 200,
place = {United States},
year = {2018},
month = {6}
}