Yes they can be. However, if you want to use a compatibility layer with them like proton the game files have to be stored in exFat (Linux file system format) format. If you have them on a drive formatted for NTFS (windows file system format) the game won’t start and wont tell you why. Games with native versions will run fine from a NTFS partition.
I'm guessing symlinking the compatdata folder to a Linux friendly filesystem, like Valve recommends here, would probably fix issues like that. I'm sure there must be edge cases but, in my admittedly not extensive experience, I haven't encountered any myself.
So currently my backups are on my media server which is ext4. These would be moved to my gaming system when I wanted to install them. I would just need to make sure that was formatted in exfat for this to work?