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The game continues shortly after the events of Assassin's Creed, where, in 2012, Desmond Miles (Nolan North) is still a prisoner at Abstergo Industries after searching the memories of his ancestor, the Assassin Altaïr, in the Animus. Abstergo, the modern-day Knights Templar, had been using Desmond to locate powerful out-of-place artifacts called "Pieces of Eden." Using the "Eagle Vision" ability he gained as a result of the "bleeding effect" (from overexposure to the Animus), Desmond is able to see messages and symbols written in blood on his bedroom wall, written by the former test subject, named "Subject 16 (Cam Clarke)". Lucy Stillman (Kristen Bell), a former researcher for Abstergo and an Assassin, frees Desmond and brings him to a secret hideout used by herself and two other Assassins, historian Shaun Hastings (Danny Wallace) and computer expert Rebecca Crane (Eliza Schneider). With their own version of the Animus, dubbed the 'Animus 2.0', they invite Desmond to help them discover the memories of his ancestor, Ezio Auditore da Firenze, for two reasons: to train Desmond in Assassin skills through the bleeding effect, and to find other Pieces of Eden.
During one break from using the Animus 2.0, Desmond suffers a hallucination that returns him to the body of Altaïr in Acre, and has intercourse with Maria, a Templar he had earlier spared (a decoy for Robert de Sable in Assassin's Creed whom Altaïr formed a relationship with in Bloodlines); when Altaïr departs, Desmond finds the memory staying with Maria (thus implying that she is now pregnant with one of his ancestors), and leaves him confused when he recovers. He also learns of the case of Subject 16, one of several previous test subjects used by Abstergo, and the person responsible for writing the images he saw in his room at Abstergo. Subject 16 has managed to hack the Animus and place twenty glyphs that can only be seen and decoded by the Animus user, revealing a video of a man and a woman, claiming to be Adam and Eve, carrying the "Apple of Eden", running through a futuristic setting identified, by a flash of binary code, as Eden.
When Desmond returns to Ezio's memory after he fought off Borgia, they find several corrupted memories, and are only able to return Desmond to Ezio's memories in the year 1499 (The memories comprise the semi-historical siege of Forli by the Orsini family and the Bonfire of the Vanities), where Borgia has since become Pope Alexander VI at Vatican City. Ezio's memories reveal that he and his allies have completed the Codex and discovered that "The Vault" lies in Rome, and realize that the Papal Staff is another Piece of Eden; Borgia's plan, upon deposition of the Medici family, would allow him to become Pope and gain access to the staff and the Vault.
Ezio travels to Rome; while his allies distract the rest of the city, Ezio discreetly enters the Vatican and attempts to assassinate Borgia inside the Sistine Chapel (while he preaches the Nicene Creed in Latin). Borgia manages to escape with both the Apple and the Staff, and attempts to use them to open the Vault, but Ezio catches up and defeats him but does not kill Borgia, since revenge will not bring back his family. In Ezio's hands, the Apple and Staff open the Vault; inside, he finds a holographic figure that identifies him as The Prophet that has brought Desmond and the 21st century observers to the Vault, much to Ezio's confusion. The figure, calling herself "Minerva" and addressing Desmond directly, reveals that she and others of her kind were part of a far more advanced society (Those Who Came Before) that lived on Earth and created humans in their own image (it is hinted several times throughout the game that humans were created as a slave race). Eventually man freed themselves and the two races went to war against one another, soon halted by a natural celestial catastrophe involving a massive solar flare which resulted in the destruction of most life on Earth. The remaining people of both races rebuilt society. The few remaining Ones Who Came Before constructed several "temples" around the world (one being located within the Vatican) that would help the human race to prevent the same disaster from reoccurring once the Ones Who Came Before had become extinct. Minerva insinuates that records of the existence of the Ones Who Came Before, as well as their warning, had been misunderstood and had, over time, evolved into various myths, legends and religions throughout the modern world. As the hologram vanishes, Minerva says "the rest is up to you, Desmond", confusing Ezio.
As the memory ends and the credits begin to roll, Desmond wakes to find that Abstergo has discovered their hideout and, with his assimilated skills from Ezio and Altaïr, he manages to escape with Lucy and the others. As the scene fades to black with the credits still rolling, they take a van with an Animus 2.0 built inside. Lucy then explains that Minerva was referring to a great celestial catastrophe. She goes on to explain that a weakness in the Earth's magnetic field has been discovered, and that a single solar flare could cause worldwide disaster. This hints towards the 2012 Doomsday prediction. Desmond prepares to re-enter the Animus as the game ends, which allows the player to continue as Ezio after the game has finished.