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Narumi Katou, in a bear costume promoting the Straw Circus, encounters Masaru Saiga, who accidentally triggers Narumi’s Zonapha attack. Masaru’s laugh saves Narumi, but he’s kidnapped by men in black suits. Narumi rescues him, escaping by train. Masaru shares his father’s death and inheritance tied to Karakuri puppets. On the train, they’re attacked by puppets, revealed when one is destroyed. Masaru summons Shirogane, a harlequin-clad woman, who uses the puppet Harlequin from his suitcase to defeat the attacker. Shirogane takes Narumi and the unconscious Masaru to a clinic, while a pursuer deploys the puppet Pulcinella.

Ashihana sends Pulcinella to attack, but Shirogane’s Harlequin easily defeats it. Ashihana’s gang captures Masaru, but Narumi rescues him, suffering a Zonapha attack. Unable to make Shirogane or Masaru laugh, Narumi gets Shirogane to beat him up in a store, curing his attack. Shirogane and Masaru move into Narumi’s apartment, unaware they’re being watched. The puppet Grimaldi snatches Masaru through a window. Ashihana, from the Slaughter Team, reveals the Kidnap Team took Masaru to the Saiga villa in Karuizawa, filled with dangerous Karakuri puppets, and offers to guide them there.

Masaru’s uncle, Zenji Saiga, claims to protect him but raises suspicions. Narumi and Shirogane storm the Saiga villa, clashing with the Kidnap Team as the Slaughter Team follows. Shirogane’s Harlequin destroys a trap door and the puppet Theogualtier. Masaru discovers his father’s notes revealing he’s bait to destroy the Kuroga clan. Narumi and Shirogane fall into a trap, triggering Narumi’s Zonapha attack. Shirogane shares her past as a puppet master and why she can’t laugh. Masaru escapes Zenji by jumping from a window, landing safely near Ashihana, whom he tries to hire.

Ashihana declines Masaru’s offer until a diary reveals the Slaughter Team’s exploitation by the Saiga. Using Grimaldi, Ashihana re-enters the villa. Yamanaka traps Narumi and Shirogane, and Masaru agrees to be Zenji’s son, but attacks him when Zenji plans to kill them. Shirogane shares her tragic childhood with Narumi. Masaru and Ashihana use Grimaldi to free them, but Yamanaka attacks again. Masaru controls Harlequin, shifting the battle until explosives destroy the villa. Masaru, Narumi, and Shirogane survive, but only Narumi’s left arm remains.

Two months later, Masaru recovers and lives with Shirogane, who enrolls in a nearby high school to protect him from bullies. Masaru shrugs off their taunts, showing his scars. Shinobu Nakamachi faces eviction while rebuilding a circus. At school, Masaru gains acceptance, and Shirogane’s acrobatic talents make her popular. Masaru takes Shirogane to meet Nakamachi, convincing her to join his circus with Nori, Hiro, and animal handler Liselotte. Meanwhile, Narumi lies unconscious in intensive care, missing his left arm.

Narumi awakens in an Illinois hospital with amnesia and a prosthetic arm, saved by Guy Christophe Resh. The hospital, run by Dr. Banhart, houses 2,000 children with Zonapha syndrome, where staff smile to prevent attacks. Narumi learns terminal Zonapha patients linger between life and death. Resh reveals the Midnight Circus uses automata to spread Zonapha and asks Narumi to become a Shirogane. The last Aqua Vitae healed Narumi. When Paulmann and Anselmus attack the school, Resh uses his Karakuri Olympia, and Narumi helps defeat them.

Paulmann and Anselmus injure Narumi, but his Aqua Vitae-enhanced healing allows him to destroy them. Narumi agrees to become a Shirogane to protect the children. At the Nakamachi Circus, Shirogane performs as a clown and is challenged by Vilma. That night, Vilma corners Masaru to kill him but is stopped by Shirogane, who recovers from Vilma’s knives and defeats her with Harlequin. Impressed by Shirogane’s loyalty and Masaru’s resolve, Vilma joins the Nakamachi Circus.

Shirogane enters a beauty contest for the Nakamachi Circus’s publicity. Masaru convinces Lise to perform, while Shirogane recalls Narumi. In China, Narumi, Guy, and Lucille face ten hijacking automata on their plane. Narumi defeats them without triggering explosions. Mr. Spazza’s insectoid automata attack, and Guy exits to fight them while Lucille lands the plane in a bay. The Nakamachi Circus’s opening is disrupted by the crash. Shirogane stops the automaton Magdalen from attacking Masaru, and Narumi appears through the flames.

After the crash, Shirogane rescues Guy and shares her past with him and Narumi. Masaru, haunted by dreams, searches for Narumi. In China’s mountains, Narumi, Lucille, and Ming-Xia find Ming-Xia’s father, Liang Jian-Feng, with Zonapha at an Aqua Vitae spring. He recounts his ancestors, Yin and Jin, who studied alchemy in Prague. Narumi recognizes the story, recalling the brothers’ love for Francine, which caused their rift.

Narumi recounts Yin’s memories: Jin abducted Francine after she chose Yin. Years later, Yin found Francine imprisoned in Quiberon, dying from a disease. He perfected Aqua Vitae to save her, but she died in a fire. Jin later created an automaton, Lady Francine, animated by Aqua Vitae, and spread Zonapha to force villagers to make her laugh. Lucille, a survivor, gained Yin’s memories and Harlequin, vowing to destroy Jin’s automata. Pantalone seeks Aqua Vitae, but Liang Jian-Feng triggers an explosion, destroying the spring.

In Maine, Shirogane-Os prepare to attack the Midnight Circus in the Sahara. Narumi, Lucille, and Ming-Xia join them, meeting George Laroche and Ashihana in France. At the circus, they face the Faceless Commander and his Shirogane-Os. Les Quatre Pionniers propose one-on-one battles. Zed destroys two automata but is defeated by Merry-Go-Round Olsen. Narumi smashes an automaton, while Fatima and Ming-Xia face Orazio and Pedrolino. After winning, a trapdoor sends them to another challenge.

Fatima and Ming-Xia receive treatment, while Narumi, Rockenfield, Malina, and Tor face deadly traps in the Midnight Circus. They split into two groups, with Narumi’s group navigating a dark staircase. The others enter a chamber requiring combat to proceed. George and Ashihana arrive by helicopter. Below, Narumi’s group faces more traps, and the Faceless Commander sacrifices himself to save Narumi, who reunites with Tor, Timbavati, Rockenfield, and Malina to confront Les Quatre Pionniers.

Tor, Timbavati, Rockenfield, and Malina battle the Quatre Pionniers. A weakened Narumi struggles to reach Doll Francine. Lucille arrives with Fatima, Ming-Xia, Ashihana, and George, unveiling her Francine marionette, Angelina, halting the circus. Lucille convinces Dottore to abandon Francine, but he fatally wounds her, causing her to crystallize. Tor self-destructs to eliminate automata, allowing Narumi’s treatment. Timbavati battles Columbine, using his Shirogane blood to neutralize her, but both die.

Pantalone and Arlecchino destroy the Francine marionette and George. A Shirogane doctor dies saving Narumi. Fatima’s Spinettina fails against Pantalone and Arlecchino, but Narumi defeats them. Lady Francine reveals she’s a copy, and the real Francine is elsewhere. Narumi attacks Shirogane, mistaking her for Francine based on a Clogue survivor’s claim, but spares her after recalling their past with Masaru.

At the Saiga ruins, Masaru receives a letter and keys from Sadayoshi, revealing he’s his father reborn. Kuroga puppeteers attack with Shogetsu, believing Masaru is Sadayoshi. Masaru uses Goyellemes and Captain Nemo to defeat them but is captured and brought before Shōji’s conscious remains.

Shōji forces Masaru to drink his blood, triggering memories of Shōji’s past at Miura Dojo and meeting Angelina (Tohno-dayu), who wielded Arlequin. Shōji drank Aqua Vitae to stay with her forever, vowing eternal love.

Shōji reveals Sadayoshi was adopted, not his biological son. Guy shares his Zonapha infection and transformation into a Shirogane. Angelina refused to surrender her Soft Stone, defeating Guy. Shōji adjusted a Francine automaton to be less powerful and brought her home to Angelina, who later gave birth to a daughter.

Shōji names his daughter Éléonore. Her birth affects Guy and Francine, who feels incomplete without a vital gear. Automata attack for the Soft Stone, now in Éléonore. Francine escapes with her, turning well water into Aqua Vitae, consuming herself. Angelina dies fighting automata, crystallizing. Shōji and Guy continue the battle.

Guy insists Masaru is Sadayoshi. Masaru denies it, encountering Éléonore but falling unconscious after Guy’s attack. Shōji’s memories reveal Éléonore’s life in Quiberon and Sadayoshi’s betrayal, using Masaru for immortality. Shōji destroyed the memory data, surviving Sadayoshi’s attempt to kill him.

Masaru recalls Sadayoshi downloading memories into him during a car crash, where Shōji and Guy intervened. At Karuizawa, Daiki, the Faceless Commander, claims to be Masaru’s father, embodying Bai Jin and Sadayoshi. He attacks, but Éléonore takes a blow meant for Masaru. Daiki escapes with her, challenging Masaru to follow. Shōji dies, reuniting with Angelina in the afterlife.

Masaru mourns Shōji as villagers succumb to Zonapha. The Faceless Commander, Deus, unleashes Artemis, composed of Apollyon bugs. Masaru and Guy pursue, but Cupidia downs Guy. Narumi destroys Cupidia and joins Guy to reach the Zonapha Research Institute, where Fou’s “Harry” can counter Apollyon. Faceless’ automata attack, and Arlecchino, Pantalone, and Colombine discover Éléonore resembles Francine.

Ming-Xia defeats Gambler Jones to save Tom. George calms children with music but faces Bola Misteriosa. Ashihana challenges Pantalone, who spares him, recalling Francine’s orders.

Ashihana uses George’s Shirogane blood to fight Pantalone, who spares him. George defeats Bola Misteriosa but dies. Narumi destroys automata, reaching Dr. Banhart’s lab with Ming-Xia, confronting Blom Blom Low and Drill September. Guy and Olympia hold off automata outside.

Narumi and Ming-Xia defeat Blom Blom Low and Drill September. Ashihana spares Pantalone, who helps Guy. The Long-legged Clown Express rescues survivors, including “Harry.” Masaru and Lise chase Faceless’s airship.

Masaru and Lise crash on Mont Saint-Michel. Aboard Faceless’s airship, Éléonore meets automata like Captain Graziano. On the island, Dr. Lao’s beasts attack, but Naya Steele helps Masaru after disabling Colombine. Masaru discovers the Shirogane-O’s human bodies.

Lise tames Dr. Lao’s beasts, killing him. Faceless beats Éléonore to possess Masaru. Colombine shows Masaru the Shirogane-O’s bodies. Naya attacks, but Masaru disables her. Faceless confronts Masaru with new automata.

Masaru fights Faceless’s automata with Harlequin. Lise and Colombine battle to stop Faceless’s rocket. Faceless tries to transfer his consciousness into Masaru but fails due to Masaru’s resistance.

Masaru resists Faceless’s control, using Éléonore’s blood. Colombine fights Diamantina’s teddy bears. Masaru frees Éléonore, leaving Faceless in the rocket. Narumi arrives, finding Colombine’s remains after her sacrifice.

Éléonore proves her loyalty by sharing Aqua Vitae with Zonapha sufferers. Faceless threatens to kill humanity with Apollyon. Fou plans to send “Harry” to stop him. Narumi mistrusts Éléonore.

Guy challenges Narumi over Éléonore but is dying. Masaru learns Narumi is alive and searches for him. The Nakamachi Circus heads to the launch pad with “Harry,” while Guy sacrifices himself to stop automata.

Vilma equips the Nakamachi Circus with Éléonore’s blood-tinted knives. Automata attack the train, and Vilma dies fighting Wild West Jane. Masaru destroys Keniss.

Shinobu consoles Masaru, revealing Éléonore’s sacrifices. The Nakamachi Trio prepares to fight Lady Spider and Captain Graziano. Arlequino and Pantalone seek Éléonore’s permission to stop Bringhella and Harlequin.

The Nakamachi Trio distracts Lady Spider with circus tricks, killing her with Vilma’s knife. Arlequino and Pantalone fight Bringhella and Harlequin, who confesses his love for Éléonore, tearing Pantalone apart.

Éléonore fights Harlequin to protect Narumi. Narumi defeats Bringhella. Masaru beats Captain Graziano. At the launch pad, Narumi and Masaru fight automata, with Masaru defending Narumi’s rear.

Masaru blinds Narumi to take his place in the shuttle. Narumi and Éléonore defeat Harlequin and declare their love. Ashihana dies stopping Pinball-K. Masaru confronts Faceless, who cloned Bai Jin’s body.

Faceless refuses Masaru’s plea for the Zonapha cure. Diamantina destroys Francine automata but is dismantled. Faceless helps redirect the crashing station, revealing Éléonore’s singing cures Zonapha. Masaru escapes, and humanity is saved. Six years later, Narumi and Éléonore’s circus brings joy to war-torn areas, and Masaru saves children in a bear suit.