Dave, 
1. You wrote "A - has many cascading IMAP folders with a total volume of 
>10GB".  Roughly how many folders, and do what depth?
2. Have you determined what cause the high open file usage?
3. Does it still happen when using a current version of Thunderbird?

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https://bugs.launchpad.net/bugs/808752

Title:
  GLib-ERROR **: Cannot create pipe main loop wake-up: Too many open
  files

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