Takayama Naoto is a high school second-year who dreams of being a train conductor. In hopes of getting a job with Japan National Railways, one of the most stable businesses in Japan due to government support, Naoto has applied to an on-the-job training program for students.

After seeing the others back to Tokyo while they cleaned up the aftermath of the Hokutosei incident, Naoto and Iida wait at Aomori Station. The engine that will pull their train to Tokyo is the KiHa 381, equipped with a pendulum-style, diesel-fueled gas turbine engine. Shortly after they depart, Naoto hears a strange sound and can't shake the feeling that something isn't right.

Naoto and the others managed to fight off their attackers on the Hokutosei, but while on the run, Naoto and Bernina find themselves under attack again. This time it's Aoi who comes to the rescue after catching up with them in Sendai via the Tohoku Shinkansen. Just as he breathes a sigh of relief, Naoto's phone rings...

Sassho Mari, like Naoto, is a second year at Kiryu Railway High School. She's into cooking, cleaning, doing laundry, and collecting recordings of train sounds. In hopes of working as an attendant in a railway-related company, she's begun on-the-job training with JNR's subsidiary, Japan Restaurant Enterprise Co., Ltd.

Prince Bernina of the small Mediterranean kingdom of Atella has arrived in Japan to attend a sister city ceremony in Sapporo, and the K4 members are appointed to guard and guide him on his way there. Naoto and the others are about to board the Hokutosei 3 at Ueno Station when Aoi contacts Naoto and tells him she's pursuing a suspicious man who was watching the platform.

Having qualified for on-the-job training, Naoto is assigned to K4, the Tokyo Central Railway Security 4th Guard Team. Waiting for him there are his partners from JNR Central Academy: Aoi, Haruka, and Sho. They immediately set about their work at Tokyo Station, but as if being teamed up with the gruff Aoi didn't worry him enough, Naoto is increasingly anxious as he watches the Tokyo Public Security Mobile Police set out on a mission.

Early in the morning, Naoto is dragged into shooting practice with Aoi beneath Tokyo Station. When they finish, Aoi still doesn't seem satisfied. Then Naoto gets a message from Mari about plans for their school's trip the next day.

The members of K4 have been punished with at-home suspension for their reckless actions on the Ashio Line. Naoto is relaxing at home when he receives a note in the mail that turns his mood upside-down: an anonymous death threat. He calls Aoi for advice, but there's no answer.

Naoto and K4 head toward Yokokawa as the rain plummets down. Haruka says the track from Usui Bridge No. 3 to Yokokawa should be safe since it's regularly maintained for the opening of the Usui Abt Railway, but the downgrade is steep, they can't slow down, and the narrow tunnels make it difficult to handle curves... They're in a serious pinch when Iwaizumi takes action!

The popular idol Kashima Noa is named the honorary railway security team leader for the day, and K4 is appointed to guard her. They accompany Noa on the Odoriko special express to a JNR-sponsored event taking place on a beach near Ito Station.

Naoto and the other K4 members head to Karuizawa for Advanced Railway Security Force Training. Naoto is excited to hear that they'll have a course on operating an EF63 electric locomotive. Aoi accompanies him in shooting lessons and strength training, saying she doesn't want him to slow her down as they'll be working in railway security together, but Naoto tells her he's aiming to be an engineer instead, leading to an argument.

Misunderstandings further threaten the harmony among the K4 members. Even the weather is on a rampage, causing a landslide near Karuizawa. Meanwhile, an employee of the Japanese Organs Transit System tells station attendants that she must get an organ to the hospital in Maebashi as quickly as possible for a transplant operation, but both railways and roads are closed due to the heavy rains.