<span class="paragraphSection"><div class="boxTitle">Abstract</div>Temperature stress is a fundamental challenge for all organisms. While two-component systems (TCSs) are known to transduce environmental signals in microbes, their role in thermal sensing remains underexplored. Here, we unveil a novel thermosensitive TCS, DhqSR, in the thermophile <span style="font-style: italic;">Thermus thermophilus</span> HB27. We demonstrate that the histidine kinase DhqS perceives thermal cues and autophosphorylates at His327. Its cognate response regulator, DhqR, is activated through a unique tyrosine-phosphorylation mechanism: phosphorylation at a unique Tyr84 residue, rather than the canonical aspartate. This atypical DhqSR system orchestrates cellular thermoadaptation by directly regulating a key enzyme in the shikimate pathway, type II 3-dehydroquinate dehydratase (DHQase). Our findings reveal a novel molecular mechanism of temperature sensing and adaptation, providing a new paradigm for microbial environmental adaptation and offering a unique toolbox for engineering thermotolerance.</span>