<p>Lichens, comprising filamentous fungi and algae/cyanobacteria engaged in mutualistic symbiosis, exhibit remarkable adaptability to environmental challenges. While fungi safeguard algae from dry conditions, their ability to mitigate other stresses remains uncertain. Additionally, the functions of coexisting bacteria within lichen communities remain relatively unexplored. This study investigates the potential of indole-3-acetic acid (IAA) as a stress-response signaling molecule in lichen symbiosis. We subjected IAA-treated monocultures of algae and co-cultures of the fungal–algal complex to various stress conditions. IAA’s role in bolstering resilience was evident, as demonstrated by the release of IAA (0–500 µM) by bacteria isolated from the lichen <i>Parmelia tinctorum</i>. This IAA was subsequently utilized by the lichen photobionts to alleviate oxidative stress. IAA acted as a communication signal, priming algal cells to defend against impending stressors. Further microscopic examinations unveiled that only the fibrous extensions were exposed in fungal cells that were in direct physical contact with viable algal cells. Co-cultivation and subsequent microscopic observations revealed that the algal cells were protected from diverse stressors by a barrier of fungal hyphae. Our findings underscore the significance of IAA in enhancing stress resistance within the context of lichen symbiosis, thereby advancing our understanding of the adaptability of these unique organisms. Further exploration of bacterial functions in lichen symbiosis holds promise for uncovering novel insights into their ecology and biology.</p>