This is the issue (I reported it and can reproduce it):
kobolabs/Kobo-Reader#70. It happens on macOS and linux, maybe windows. It is the source of the intermittent I/O Error issues, and is also why some USB ports stop working after using it with the kobo.
This can temporarily worked around by using a different USB port or rebooting, but it will eventually come back. Please comment on the issue if it affects you, as kobo seems to be reluctant to try to fix it (I've tried contacting them), and gtalusan (the main person in charge of the GitHub repo) is being silent.