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Quebec police arrested Thomas Harding, the engineer and train driver, and two other train workers - Jean Demaitre and Richard Labrie - on Monday. They were each charged with 47 counts of criminal negligence causing death.
The same charges were made against the railway company, Montreal, Maine and Atlantic Railway Ltd (MMA), which filed for bankruptcy protection last year. No individual executives were named.
The three accused were escorted to the court in handcuffs in the tiny town of Lac-Megantic, where the train carrying oil from the Bakken oil fields derailed and exploded on July 6, 2013. The fire engulfed a busy night club and flattened much of the town's center.
Residents, including some who lost family members in the disaster, stood and watched quietly as the men were paraded past news cameras. Some 30 people entered the court room.
The case will resume on September 11 when the suspects enter their pleas. The maximum penalty is life in prison, although experts say much shorter sentences are likely.
Lawyer Thomas Walsh said his client Harding, who has been at the center of the investigation, planned to plead not guilty to the charges and ask for a trial by jury.
Walsh criticised Quebec police for their commando-style arrest of Harding on Monday in his back yard, swooping in with what he described as a SWAT squad and sirens at full volume. Harding has cooperated fully with police and was willing to turn himself in voluntarily if and when charges were laid, he said.
"It was like trying to kill a fly with a cannon. It wasn't necessary," he said.
Although there were no charges against Ed Burkhardt, the chief executive officer of MMA, the accusations against the company as a whole signaled that the prosecutor could eventually target senior management for blame, said Gilles LeVasseur, a professor of business law at the University of Ottawa.
That could take longer because Burkhardt resides in the United States. The prosecutor may also be hoping the three employees cooperate by providing information on the company's safety practices in exchange for lighter sentences.
"What you really want is the top executives, to get a message to management that leadership is responsible for the security and well-being of society and it's not just downloading it to lower people in the organization," LeVasseur said.
Harding has been the main focus of the probe into the disaster, one of several recent accidents involving oil transport by rail that have sparked a regulatory crackdown on the industry in Canada and the United States.
He was the single engineer on the train, which he had parked for the night on a main line, uphill from the small town. At some point in the evening, firefighters were called in to put out a small fire in the train's engine.
The train later broke loose and careened down into the town where it leapt off the tracks and exploded.
The railway initially blamed the catastrophe on the failure of the train's pneumatic airbrakes after the engine fire. Burkhardt later said Harding did not apply an adequate number of handbrakes to hold the train in place.
Labrie was a traffic controller and Demaitre was a director of operations at MMA.
A website created to raise funds for Harding's defense describes him as having spent 33 years working on the railroad, following in his father's footsteps.
"Tom Jr. comes from a family that has a lot of heart and soul," the site says. "Megantic has wounded him deeply. He will never be the same man."