Abstract
EnvZ and OmpR constitute the bacterial two-component signal transduction system known to mediate osmotic stress response in a number of Gram-negative bacteria. In an effort to understand the mechanism through which Shewanella oneidensis senses and responds to environmental osmolarity changes, structure of the ompR-envZ operon was determined with Northern blotting assay and roles of the EnvZ/OmpR two-component system in response to various stresses were investigated with mutational analysis, quantitative reverse transcriptase PCR (qRT-PCR), and phenotype microarrays. Results from the mutational analysis and qRT-PCR suggested that the EnvZ/OmpR system contributed to osmotic stress response of S. oneidensis and very likely engaged a similar strategy employed by E. coli, which involved reciprocal regulation of two major porin coding genes. Additionally, the ompR-envZ system was also found related to cell motility. We further showed that the ompR-envZ dependent regulation of porin genes and motility resided almost completely on ompR and only partially on envZ, indicating additional mechanisms for OmpR phosphorylation. In contrast to E. coli lacking ompR-envZ, however, growth of S. oneidensis did not show a significant dependence on ompR-envZ even under osmotic stress. Further analysis with phenotype microarrays revealed that the S. oneidensis strains lacking a complete ompR-envZ system displayed hypersensitivities to a number of agents, especially in alkaline environment. Taken together, our results suggest that the function of the ompR-envZ system in S. oneidensis, although still connected with osmoregulation, has diverged considerably from that of E. coli. Additional mechanism must exist to support growth of S. oneidensis under osmotic stress.
Highlights
Osmotic stress caused by changes of environmental osmotic strength is among the environmental stresses of great physiological relevance to microbes [1]
Two-component signal transduction systems composed of a sensory histidine kinase and a response regulator are broadly utilized by bacteria for effective acclimation to environmental changes
Given the number of studies aiming to dissect stress responses of S. oneidensis performed, it is surprising that the Arc two-component system is the only one being scrutinized [23,24,25]
Summary
Osmotic stress caused by changes of environmental osmotic strength is among the environmental stresses of great physiological relevance to microbes [1]. To cope with osmotic stress, bacteria have developed a number of strategies for effective adaptation. These strategies and their underlying mechanisms have been extensively reviewed [2,3]. In Escherichia coli, it is known that the EnvZ/OmpR two-component system plays a central role in mediating signal transduction in response to osmotic stress [4,5,6]. Environmental osmolarity affects the porin composition by the sum of EnvZ kinase and phosphatase activities in vivo [8]. Deletion of EnvZ/OmpR was reported to have an impact on expression of more than 100 genes in E. coli, causing drastic changes in cell growth and important cell functions such as metabolism and motility [16]
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