Autobot Cliffjumper is killed by the decepticon's commander Starscream. In Jasper, Nevada, two young humans—Jack Darby and Rafael Esquivel—are accidentally caught in the crossfire of a fight between giant, mechanical aliens that transform into ordinary vehicles. The two kids are taken to the base of the Autobots, where the Autobot leader Optimus Prime explains that he and his team are a race of autonomous robotic organisms from the far-off planet Cybertron, and they are fighting over their life-source, Energon, with the Decepticons, with whom they once had a war.

Debuts: Optimus Prime, Arcee, Bumblebee, Bulkhead, Ratchet, Cliffjumper, Jack Darby, Rafael Esquievel, Miko Nakadai, Sierra, Megatron, Starscream, Soundwave and Vehicons

The Decepticon leader Megatron returns from a three-year exile with a plan to exploit the properties of a mysterious substance called "Dark Energon", which has the ability to turn the bodies of dead Transformers into zombie-like Terrorcons. The Autobots storm an Energon mine in search of their lost comrade Cliffjumper, only to discover that his dead body has been revived as a ravenous zombie by Dark Energon.

Optimus Prime and Ratchet head out to investigate Megatron's activities while Arcee and Bumblebee go on patrol, leaving Bulkhead with Jack, Miko and Rafael at the base. Meanwhile, Soundwave kidnaps the human Agent William Fowler, with Starscream wishing to learn the location of the Autobots' base.

Bulkhead, Arcee and Bumblebee sneak on to the Decepticon warship, the Nemesis, to rescue Agent Fowler, while Optimus Prime and Ratchet fight off Megatron and a horde of Dark Energon zombies.

Following Megatron's supposed demise, Starscream appoints himself as the new Decepticon leader. However, to his annoyance, he finds that the troops don't respect him as much as they did Megatron and are weary towards him becoming leader. In order to gain their respect, Starscream awakens Skyquake, a legendary Decepticon warrior who was entombed in stasis on Earth for centuries, and attempts to recruit him into his new army. Meanwhile, Ratchet agrees to help Jack, Miko and Rafael with their school science projects, with explosive results.

While on a scouting mission in the Arctic, Bulkhead and Bumblebee find a crashed space pod buried in the ice. They bring it back to base for examination, and Optimus Prime and Arcee venture out into the Arctic to find clues on the pod's origin. While they are out, the other Autobots discover that the pod contains a large swarm of Scraplets, a vicious and highly dangerous form of Cybertronian wildlife that eats metal. The Scraplets infest the Autobot base, devouring any metal in sight and damaging the Ground Bridge, leaving Optimus and Arcee stranded in the Arctic.

The Autobots receive a message from Wheeljack, an old friend and partner of Bulkhead's from the days of the war, who is visiting Earth while journeying across the galaxy. Upon picking up the message's signal, Starscream and Soundwave capture Wheeljack before he can meet the Autobots, and they send in Makeshift, a Decepticon spy able to take on any form, disguised as Wheeljack to discover the location of the Autobot base.

Debuts: Wheeljack and Makeshift

Agent Fowler asks for the Autobots' assistance in transporting a powerful nuclear device to a military base, but since sending such a device through the Ground Bridge could be potentially dangerous, they have to travel by road. Along the way, the Autobots are ambushed by M.E.C.H., a terrorist organization who wish to steal the nuclear device and use it for their own nefarious purposes. And to make things worse, the Decepticons get involved as well.

The Autobots discover that an Energon Harvester, an ancient and powerful device from Cybertron's distant past, is on display in a museum, and they attempt to retrieve it with Jack, Miko and Rafael's aid before it falls into the wrong hands. Starscream also learns of the Harvester's whereabouts, and he sends Soundwave, along with new Decepticons Knock Out and Breakdown, to obtain it.

In an attempt to get even with school bully Vince, as well as impress his crush Sierra, Jack convinces Bumblebee to help him win an illegal street race. However, things go awry when Knock Out gets involved in the action, kidnapping Vince in the belief that he is Bumblebee's human partner.

Jack accompanies Arcee on a routine scouting mission in a forest, where they discover a crashed space ship. They soon discover that the owner of the ship, the deadly and ruthless Decepticon sadist known as Airachnid, is still prowling the forest in search of a human to hunt, putting Jack in danger and causing Arcee to have visions regarding her last encounter with Airachnid on Cybertron during a mission with her partner Tailgate.

Debuts: Airachnid and Tailgate (flashbacks)

Megatron sends Starscream and Airachnid to the site of a crashed Decepticon ship to recover the Immobilizer, a powerful weapon with the ability to freeze Transformers in their tracks. But after the Autobots discover that Starscream has been double-crossed by Airachnid, they are surprised when Starscream states that he wishes to join them...

Optimus Prime recites a passage from the Covenant of Primus, detailing a doomsday prophecy connected to Earth and involving Megatron. After Megatron attacks Rafael and Bumblebee, leaving Rafael unconscious and severely injured, Optimus realizes that he can't end the Autobot-Decepticon conflict diplomatically, and decides to confront Megatron and destroy him once and for all.

With the help of information from Starscream, the Autobots commandeer the Decepticons' space bridge to send Jack and Arcee to the Transformers' home world of Cybertron, with a plan to use the information stored in Vector Sigma to restore Optimus' memories. Meanwhile, after a run-in with Starscream (whom Megatron claimed was dead), Orion wonders if Megatron is telling him the whole truth.

On Cybertron, while searching for Vector Sigma, Jack and Arcee are attacked by an Insecticon and a swarm of Scraplets. On the Nemesis, Orion becomes ever more curious about who he really is, so he begins to rebel against Megatron and uncover the elaborate lies put in front of him. Later, Megatron distracted by Arcee fails to prevent Jack from endowing the knowledge acquired from the Vector Sigma, and Optimus regains his lost memory but loses what he had acquired during his stay on the Nemesis.

Wheeljack returns to Earth in pursuit of the Decepticon Dreadwing, Skyquake's twin brother who is responsible for the death of the Wrecker Seaspray, and asks for Team Prime's help in apprehending him. While Bulkhead is excited about seeing his best friend again, Optimus Prime soon becomes concerned with Wheeljack's recklessness, aggression, and disregard for civilians during their search for Dreadwing.

Debuts: Dreadwing and Seaspray

Megatron sends Breakdown, Airachnid and Dreadwing in search of Energon in a forest, with Airachnid unaware that her comrades have actually been ordered to terminate her for treason. She catches on to the plan and flees, killing Breakdown in the process, and upon encountering a lone Insecticon, she uses her abilities to control it, and challenges Megatron to a fight to the death, but not before having it attack Starscream. Starscream passes on the Insecticon's presence on Earth, leading to the Autobots becoming involved and another face-off between Arcee and Airachnid.

M.E.C.H. produces a clone of Optimus Prime (which Miko off-handedly names Nemesis Prime) and sets it loose on a military base, where it wreaks havoc. The United States Military immediately attributes the chaos to the real Optimus, and order the Autobots be shot on sight. While Agent Fowler tries to convince his superiors that Optimus did not attack the base, Team Prime tries to track down Nemesis Prime and clear their names.

Debuts/Deaths: Nemesis Prime

Agent Fowler is forced to explain recent events to his superior, General Bryce. Threatened with a military tribunal and Team Prime's termination, Fowler tries to convince Bryce that the Autobots are still on the military's side, but Bryce believes that Optimus went rogue and has perished, failing to fully understand that Nemesis Prime was not the real Optimus.

Bulkhead accidentally becomes trapped on board the Nemesis while on a scouting mission, and tries to escape without being discovered. Meanwhile, Starscream and Airachnid send their newly-gained armies (Starscream's being five clones of himself, and Airachnid's being a hive of Insecticons) to the Nemesis, both intending to kill Megatron.

Bulkhead goes to a volcanic island on the Equator to find the fourth and final Iacon relic. But to his horror, he discovers that the relic is a piece of Tox-En, a form of highly toxic Energon that is lethal to Transformers. He tries to dispose of the Tox-En by throwing it into a volcano, but it deteriorates his strength, and things are made worse when a group of Insecticons led by Hardshell arrive in search of the relic.

Bulkhead is left in a critical condition and on the verge of death after his fight with the Insecticons and exposure to Tox-En. Distraught about what has happened to their friend, Miko and Wheeljack head out to find Hardshell and get revenge.

Miko becomes frustrated with Bulkhead's slow recovery and storms out of the base. Finding Miko weeping by herself, Arcee tries to cheer her up by telling the story of how she and her last battle partner Cliffjumper first came to Earth. Starscream had captured Arcee and Cliffjumper and took them to be interrogated by the Decepticon scientist Shockwave, and upon escaping they discover Shockwave's plan to build a space bridge to Earth.

During a fight with the Decepticons, Team Prime is unexpectedly aided by Smokescreen, a young and impulsive Autobot. Despite Arcee and Ratchet's distrust in the newcomer, Optimus Prime invites Smokescreen to the base for further training. Meanwhile, Starscream discovers that a meteorite of Red Energon (which grants the consumer enhanced speed) has crashed on Earth, and sets out to claim it for himself.

M.E.C.H. scientists implant the dying Colonel Leland Bishop (aka Silas) into a battle armor and life-support system made from Breakdown's dead body. Silas kills the scientists and approaches Megatron, introducing himself as C.Y.L.A.S. (Cybernetic Life Augmented by Symbiosis), asking for a position in the Decepticon ranks and offering to aid their cause with Project: Damocles, a satellite-based laser weapon system of his own invention.

Optimus Prime discovers that the Star Saber is embedded with a message from his former mentor Alpha Trion. In this message, Alpha Trion explains about four Iacon relics called the Omega Keys, which when brought together are able to make Cybertron inhabitable again. Meanwhile, Megatron opens the tomb of one of the late thirteen original Prime on Cybertron, taking an arm and having it attached to him so he can use the Forge of Solus Prime to build a Dark Energon weapon strong enough to counter the Star Saber: the Dark Star Saber!

Disillusioned with the Decepticon cause for letting Starscream back to their ranks, Dreadwing offers the Forge of Solus Prime to the Autobots. He then seeks revenge on Starscream for desecrating his twin, but Megatron kills him to reluctantly save Starscream. As Megatron subsequently unleashes his forces on Cybertron, Optimus Prime uses the Forge to upgrade the ground bridge into a space bridge. Armed with every Iacon relic they have, the Autobots head to Cybertron to find the Omega Lock, the device needed to restore Cybertron with the Omega Keys.

Megatron activates the Omega Lock and starts restoring Cybertron, but he then reveals he is also going to use the Lock's power to turn Earth into a mechanical planet - which would kill all of its inhabitants. Optimus Prime destroys the Lock before it can finish its restoration, saving Earth but dooming Cybertron. The Autobots retreat back to Earth, only to find a gigantic fortress has appeared outside their base - which makes it clear that the Decepticons have finally discovered the base's location.

As the Autobots try to re-group, Shockwave arrives in Darkmount after years of isolation on Cybertron, and is welcomed back into the Decepticon ranks. Wheeljack escapes from Darkmount and sets off to rendezvous with Bulkhead and Miko, unaware that Starscream has planted a tracking device on him.

The Autobots attack Darkmount in an attempt to disable its firepower to allow human military to destroy it. As Optimus prepares to join with the AllSpark, Smokescreen uses the Forge to repair him, and makes him a new, more powerful body. Optimus joins the Autobots at Darkmount and, with human support, destroys the fortress.

Final Appearances: Decepticon Miners and Alpha Trion

The Autobots adjust to new group dynamics within their expanded team and Optimus Prime scans a new vehicle form, but Smokescreen privately starts to regret not becoming a Prime. The Decepticons, having found fossilized Predacon bones on Earth, launch a scheme to clone an army of Predacons through the same method that created Predaking.

Knock Out is researching Ratchet's incomplete Synthetic Energon formula, and is using C.Y.L.A.S., still implanted within Breakdown's corpse, as a test subject. The formula makes C.Y.L.A.S. extremely aggressive, so Starscream suggests injecting him with Dark Energon to make him easier to control. However, the mixture of the two Energons turns C.Y.L.A.S. into a mindless vampire craving fresh Energon, and he wanders the ship infecting any crew member he encounters by draining their Energon. During the chaos, Soundwave banishes Airachnid and the Insecticons from the Nemesis, and the episode ends with the infected Airachnid feasting on the Insecticons to survive.

Deaths: Silas/C.Y.L.A.S. Final appearances: Airachnid and Insecticons

The Decepticons hold Ratchet captive, and Megatron attempts to persuade him to help complete the Synthetic Energon formula and restore Cybertron. Rafael and Wheeljack build a flying drone and attach Laserbeak's transponder (which Smokescreen shot off) to it, in the hope that Laserbeak's navigation systems will lead the Autobots to Ratchet so they can rescue him.

Ratchet reluctantly agrees to help the Decepticons perfect the Synthetic Energon formula, but he sabotages the project and tries to escape from the Nemesis. The Autobots launch their drone and Optimus Prime follows it, but is confronted by Starscream and the drone is destroyed. Megatron leaves Ratchet at the mercy of the vengeful Predaking, but Ratchet helps the Predacon realize that the Decepticons were behind the destruction of his army. Predaking attacks Megatron but is ejected from the ship, giving Ratchet enough time to contact the Autobots and provide the ship's location.

Deaths: Chip

The Autobots storm the Nemesis and try to reach the Omega Lock before the Decepticons can activate it and cyberform Earth. As the other Autobots fight off the Decepticon army, Jack, Miko, and Raf trap Soundwave in the Shadowzone, Optimus Prime and Megatron engage in a final showdown. During their clash, Megatron fatally shoots Bumblebee, but the scout is revived by the Omega Lock's Cyber Matter and kills Megatron, regaining his voice. Starscream and Shockwave escape, and the Autobots restore Cybertron. Saying farewell to their human allies and Ratchet, who decided to remain behind, the Autobots leave Earth to begin rebuilding their home.

Deaths: Megatron and Bumblebee (revived)

Unicron has taken over Megatron's body to get revenge on the Autobots and destroy Cybertron, and it is up to the Autobots, the Decepticons and the Predacons to form an alliance to stop him.

Debuts: Darksteel and Skylynx Final Appearances: Optimus Prime, Bumblebee, Arcee, Bulkhead, Wheeljack, Ultra Magnus, Smokescreen, Ratchet, Megatron, Shockwave, Starscream, Knockout, Vehicons, Unicron, Predaking, Darksteel and Skylynx