Feeding on compatible solutes: A substrate-induced pathway for uptake and catabolism of ectoines and its genetic control by EnuR.
Ectoine and 5-hydroxyectoine are widely synthesized microbial osmostress protectants. They are also versatile nutrients but their catabolism and the genetic regulation of the corresponding genes are incompletely understood. Using the marine bacterium Ruegeria pomeroyi DSS-3, we investigated the utilization of ectoines and propose a seven steps comprising catabolic route that entails an initial conversion of 5-hydroxyectoine to ectoine, the opening of the ectoine ring, and the subsequent degradation of this intermediate to l-aspartate. The catabolic genes are co-transcribed with three genes encoding a 5-hydroxyectoine/ectoine-specific TRAP transporter. A chromosomal deletion of this entire gene cluster abolishes the utilization of ectoines as carbon and nitrogen sources. The presence of ectoines in the growth medium triggers enhanced expression of the importer and catabolic operon, a process dependent on a substrate-inducible promoter that precedes this gene cluster. EnuR, a member of the MocR/GabR-type transcriptional regulators, controls the activity of this promoter and functions as a repressor. EnuR contains a covalently bound pyridoxal-5'-phosphate, and we suggest that this co-factor is critical for the substrate-mediated induction of the 5-hydroxyectoine/ectoine import and catabolic genes. Bioinformatics showed that ectoine consumers are restricted to the Proteobacteria and that EnuR is likely a central regulator for most ectoine/5-hydroxyectoine catabolic genes.
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.
Annina
A
Schulz
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.|Philipps-University Marburg, LOEWE-Center for Synthetic Microbiology, Hans-Meerwein Str. 6, Marburg, D-35043, Germany.
Nadine
N
Stöveken
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.
Ina M
IM
Binzen
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.
Tamara
T
Hoffmann
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.|Philipps-University Marburg, LOEWE-Center for Synthetic Microbiology, Hans-Meerwein Str. 6, Marburg, D-35043, Germany.
Johann
J
Heider
Department of Biology, Laboratory for Microbiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, Marburg, D-35043, Germany.|Philipps-University Marburg, LOEWE-Center for Synthetic Microbiology, Hans-Meerwein Str. 6, Marburg, D-35043, Germany.
Erhard
E
Bremer
D000599:Amino Acids, Diamino / Q000378:metabolism*; D001224:Aspartic Acid / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D002244:Carbon / Q000378:metabolism; D003470:Culture Media; D026901:Membrane Transport Proteins / Q000378:metabolism; D005810:Multigene Family; D009584:Nitrogen / Q000378:metabolism; D041902:Rhodobacteraceae / Q000378:metabolism*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
D000599:Amino Acids, Diamino; D001426:Bacterial Proteins; D003470:Culture Media; D026901:Membrane Transport Proteins; D014157:Transcription Factors; C121557:hydroxyectoine; D001224:Aspartic Acid; D002244:Carbon; C045628:ectoine; D009584:Nitrogen