ALAN, Hugo, Inform 6/Z-Machine (w/ v6lib), Inform 7/Glulx (w/ Glimmr), JACL (w/ Glk), TADS 2 (HTML), and TADS 3 (HTML) all have multimedia support.
TADS 2 has a source-level debugger (but ADL, ALAN, Hugo, and Inform 6/Z-Machine all have symbolic debuggers).
ALAN, Hugo, Inform 7/Glulx, TADS 2, and TADS 3 all have multimedia interpreters for each major desktop.
TADS 2 and Inform 6/Z-Machine have Java applet interpreters (but the Z-Machine applet only works for z3/z5 games) and Inform 6/Z-Machine and Inform 7/Glulx have JavaScript interpreters.
All the programs I looked at can probably be used on Darwin, FreeBSD, and illumos as well as Linux. Let me know if I missed anything.
Java applets died a merciful death more than 10 years ago. There are JavaScript interpreters for many systems, including Z-machine, Glulx, Quest, Adrift, JACL and (partially) Hugo.
Looking at my */bin dirs, there’s also scottcom, but the story file generated is incompatible with the available Linux 'terps, and Zilf/Zapf (the current best mean for writing z3 story files, IMHO) runs well under Linux+mono.
I suspect that the pair or so of python/perl IF languages (and their respective 'terps) can run fine under Linux.
A JavaScript interpreter for Z-machine is my own “JSZM” program (later I can also make XJSZM). However, it requires some ES6 features, so some JavaScript engines may not support it (although the newest versions of Firefox and Node.js both support it, and probably so does Chromium, which uses the same V8 as Node.js does). When considering JavaScript implementations of any VM, you may also consider if it uses ES6 features and so on.
Another compiler for Z-machine is ZILF, which requires Mono to use on Linux (although I have not yet tried it myself). For Linux, there is also my interpreter ZORKMID, in C. And then there are more than just the VM systems you listed. For example, I think Inform6 can also compile into Glulx (since Inform7 compiles into Inform6), although this is probably not particularly relevant to what you are doing. Many other programs may also run in emulators such as DOSBOX or whatever.
Other VMs include OASYS (a very old VM; story file binaries are dependent on int size and byte order when used with the original OAI interpreter, although my own implementations will work regardless of int size and byte order), and TAVERN (a rather new VM, of my own invention). Compiling the original OASYS sources are probably difficult because there is an include file missing, but you can run them under DOSBOX or use my implementations. There are probably others that I have forgotten, too.
You say there is also scottcom. Is there the VM specification? Then an implementation compatible with Linux can be written, and then it will be compatible.
Actually I tried ZILF without Mono but straight WINE on Linux and it worked fine out of the box. But I would suggest Mono regardless due that you get better potential with WINE when it is fully installed, along with libraries and C sharp libraries.