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Most prokaryotic signal transduction systems and a few eukaryotic pathways use phosphotransfer schemes involving two conserved components, a histidine protein kinase and a response regulator protein. The histidine protein kinase, which is regulated by environmental stimuli, autophosphorylates at a histidine residue, creating a high-energy phosphoryl group that is subsequently transferred to an aspartate residue in the response regulator protein. Phosphorylation induces a conformational change in the regulatory domain that results in activation of an associated domain that elicits the response. Related species usually rely upon orthologous regulatory systems to orchestrate responses to a given signal. Under certain circumstances, the elicited responses are largely similar across species, indicative that orthologous regulatory systems control common cellular functions across species even if the species occupy different niches. In other circumstances, the responses are distinct, either in qualitative or quantitative terms, suggesting that the regulatory systems adopted by individual species are suited to particular habitats and lifestyles. The availability of oxygen is a major environmental factor for many microbes, in particular for bacteria such as Shewanella species, which thrive in redox-stratified environments. One of the best-studied systems involved in mediating the response to changes in environmental oxygen levels is the Arc two-component system of Escherichia coli, consisting of the sensor kinase ArcB and the cognate response regulator ArcA. An ArcA ortholog was previously identified in Shewanella, and as in Escherichia coli, Shewanella ArcA is involved in regulating the response to shifts in oxygen levels. Here, we identified the hybrid sensor kinase SO_0577, now designated ArcS, as the previously elusive cognate sensor kinase of the Arc system in Shewanella oneidensis MR-1. Phenotypic mutant characterization, transcriptomic analysis, protein-protein interaction, and phosphotransfer studies revealed that the Shewanella Arc system consists of the sensor kinase ArcS, the single phosphotransfer domain protein HptA, and the response regulator ArcA. Phylogenetic analyses suggest that HptA might be a relict of ArcB. Conversely, ArcS is substantially different with respect to overall sequence homologies and domain organizations. Thus, we speculate that ArcS might have adopted the role of ArcB after a loss of the original sensor kinase, perhaps as a consequence of regulatory adaptation to a redox-stratified environment. In contrast to the highly conserved histidine kinase ArcS, the response regulator SO_4444 is species-specific for S. oneidensis MR-1 and S. baltica OS223. Bioinformatic analyses of SO_4444 and it’s genetic context suggest horizontal gene transfer from Aeromonas species. Moreover, phenotypic mutant characterization and transcriptomic analysis revealed incorporation of the phylogenetic new component SO_4444 into the consisting regulatory network of S. oneidensis MR-1. Thus, the response regulator SO_4444 as well as the Shewanella Arc-System exemplify two evolutionary strategies changing two-component regulatory networks in bacteria.