The blue light photoreceptor cum transcription factors, Aureochromes (Aureos), are present exclusively in photosynthetic stramenopiles. Co-existence of Light Oxygen Voltage (LOV) and basic leucine zipper (bZIP) is unique to Aureos and therefore ideal to study light-dependent DNA binding or, transcriptional regulation. Further, the inverse effector-sensor topology of Aureos, resembling several sensory eukaryotic transcription factors, makes them prototypical optogenetic scaffolds. In absence of 3D data, this study aims for a thorough investigation of the bZIP domains from Aureos and others, and their interaction with substrate DNA using tools from sequence and structural bioinformatics, network theory, molecular dynamics simulation and in vitro experiments. An in depth comparison of 173 Aureo, plant and opisthokont bZIPs reveals the uniqueness and evolutionary significance of Aureos in DNA binding specificity as well as dimer stability. An all atom network analysis on representative bZIP+DNA cocrystal structures, especially the measurement of eigenvector centrality, further adds importance to hydrophobic interactions in the zipper region to stabilize bZIP dimer and facilitate DNA binding in Aureos and other bZIPs. Perhaps the most notable finding is the unique histidine substitution at the basic region of Aureos unlike any other bZIPs. Not only is this residue important for DNA binding, this can serve as a potential switch point in Aureo/bZIP evolution.