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Summary  Elucidating the mechanisms controlling the synthesis of hydroxyectoine is important to design novel genetic engineering strategies for optimizing the production of this biotechnologically relevant compatible solute. The genome of the halophilic bacterium  Chromohalobacter salexigens  carries two ectoine hydroxylase genes, namely  ectD  and  ectE , whose encoded proteins share the characteristic consensus motif of ectoine hydroxylases but showed only a 51.9% identity between them. In this work, we have shown that  ectE  encodes a secondary functional ectoine hydroxylase and that the hydroxyectoine synthesis mediated by this enzyme contributes to  C.␣salexigens  thermoprotection. The evolutionary pattern of EctD and EctE and related proteins suggests that they may have arisen from duplication of an ancestral gene preceding the directional divergence that gave origin to the orders Oceanospirillales and Alteromonadales. Osmoregulated expression of  ectD  at exponential phase, as well as the thermoregulated expression of  ectD  at the stationary phase, seemed to be dependent on the general stress factor RpoS. In contrast, expression of  ectE  was always RpoS‐dependent regardless of the growth phase and osmotic or heat stress conditions tested. The data presented here suggest that the AraC‐GlxA‐like EctZ transcriptional regulator, whose encoding gene lies upstream of  ectD , plays a dual function under exponential growth as both a transcriptional activator of osmoregulated  ectD  expression and a repressor of  ectE  transcription, privileging the synthesis of the main ectoine hydroxylase EctD. Inactivation of  ectZ  resulted in a higher amount of the total ectoines pool at the expenses of a higher accumulation of ectoine, with maintenance of the hydroxyectoine levels. In addition to the transcriptional control, our results suggest a strong post‐transcriptional regulation of hydroxyectoine synthesis. Data on the accumulation of ectoine and hydroxyectoine in  rpoS  and  ectZ  strains pave the way for using these genetic backgrounds for metabolic engineering for hydroxyectoine production.

microbial biotechnology

New insights into hydroxyectoine synthesis and its transcriptional regulation in the broad‐salt growing halophilic bacterium  Chromohalobacter salexigens