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Strangers in the archaeal world: osmostress‐responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus
Author(s) -
Widderich Nils,
Czech Laura,
Elling Felix J.,
Könneke Martin,
Stöveken Nadine,
Pittelkow Marco,
Riclea Ramona,
Dickschat Jeroen S.,
Heider Johann,
Bremer Erhard
Publication year - 2016
Publication title -
environmental microbiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.954
H-Index - 188
eISSN - 1462-2920
pISSN - 1462-2912
DOI - 10.1111/1462-2920.13156
Subject(s) - ectoine , biology , mechanosensitive channels , gene , archaea , halophile , methanosaeta , bacteria , genetics , biochemistry , microbiology and biotechnology , osmoprotectant , ion channel , receptor , amino acid , proline
Summary Ectoine and hydroxyectoine are compatible solutes widely synthesized by members of the Bacteria to cope with high osmolarity surroundings. Inspection of 557 archaeal genomes revealed that only 12 strains affiliated with the N itrosopumilus , M ethanothrix or M ethanobacterium genera harbour ectoine/hydroxyectoine gene clusters. Phylogenetic considerations suggest that these A rchaea have acquired these genes through horizontal gene transfer events. Using the T haumarchaeon ‘ C andidatus N itrosopumilus maritimus’ as an example, we demonstrate that the transcription of its ectABCD genes is osmotically induced and functional since it leads to the production of both ectoine and hydroxyectoine. The ectoine synthase and the ectoine hydroxylase were biochemically characterized, and their properties resemble those of their counterparts from B acteria . Transcriptional analysis of osmotically stressed ‘ C a . N . maritimus’ cells demonstrated that they possess an ectoine/hydroxyectoine gene cluster ( hyp‐ectABCD‐mscS ) different from those recognized previously since it contains a gene for an MscS ‐type mechanosensitive channel. Complementation experiments with an E scherichia coli mutant lacking all known mechanosensitive channel proteins demonstrated that the ( N m ) MscS protein is functional. Hence, ‘ C a . N . maritimus’ cells cope with high salinity not only through enhanced synthesis of osmostress‐protective ectoines but they already prepare themselves simultaneously for an eventually occurring osmotic down‐shock by enhancing the production of a safety‐valve ( Nm MscS ).