Sonic finds himself separated from his friends in a strange, digital world – Cyber Space - which has taken the form of Green Hill Zone. Miraculously, he manages to escape Cyber Space, and awakens all alone on Kronos Island, one of the Starfall Islands, which is full of ancient ruins where strange enemies roam. There, Sonic hears a mysterious digital voice, claiming that he has done the "impossible" by escaping Cyber Space and naming him "the Key." It gives a baffled Sonic some cryptic direction about how to save his friends: he must collect the Chaos Emeralds, destroy beings called the "Titans" and "tear down the walls between dimensions." Deciding that this guidance is better than nothing, Sonic sets out on a journey to discover all the mysteries of the Starfall Islands, rescue his friends, and discover how it all ties together, which leads to Sonic becoming locked in a race against time to defeat Dr. Eggman... or so it seems.

Ares Island
As Super Sonic approaches his destination of Ares Island, he's hit by a laser beam that knocks him back to his base form; to his further annoyance, the emeralds promptly scatter across the new island. As he sets out in search of the gems, Sonic discovers Knuckles the Echidna trapped in the same sort of prison that held Amy. Upon rescuing him, Sonic snarkily asks what Knuckles is doing so far away from home; Knuckles explains that he was exploring some of the ruins when he was transported into the island and then trapped. Sonic asks Knuckles to help him search for the Chaos Emeralds so they can go home.

Further into the island, Sonic encounters the draconic Titan known as Wyvern. It ignores Sonic until Sage appears, stating that she cannot fully control the Titan, but she can make it aggressive towards Sonic. The hedgehog is forced to escape from Wyvern's missile barrage, which Sage identifies as his "last warning" to leave - Sonic simply scoffs at the mysterious girl's apparent concept of "warning" people away. Later on, Sage tries to attack Sonic directly, only for Knuckles to jump in and block her laser blast. However, Sonic refuses to attack Sage, realizing that she is trying to protect "something...or someone" from him; Sage seems shaken, but refuses to elaborate as she vanishes once more.

As the search for the Chaos Emeralds continues, Sonic and Knuckles assist a group of Koco soldiers that were separated from their commander; this eventually leads them to witness a memory of a battle between the Ancients and an unknown enemy. Another troop of Koco are taking refuge in a temple that reminds Knuckles of the ruins on Angel Island, making him wonder if the Ancients are related to his own tribe's past. After Sonic helps him defend the temple from incoming Guardians, Knuckles admits that he envies Sonic's free-living ways and resolves to explore the world himself once he's returned to normal.

After claiming six of the Chaos Emeralds, Sonic makes his way to Wyvern, suspecting that the Titan is holding on to the last gemstone in an effort to stop him from going Super. After a dynamic ascent and aerial pursuit, he reaches Wyvern's head and becomes Super Sonic once more to engage the Titan in battle. Destroying Wyvern gives him another vision of an Ancient; this one is lamenting on the unexpected demise of a comrade. Rendezvousing with Knuckles, who brags that he would've beaten Wyvern sooner if he were able to go Super, Super Sonic tells him that he has one more Titan to defeat so they can all return back to normal; he expresses worry for the missing Tails, but Knuckles assures him that the fox will be alright.

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