What will cause ..require roles [role:system.admin, role:cms.admin]?

Our editors randomly get this error while saving parts. Doesn’t seem to be any problem with the roles on the site or user. All our editors have cms.cm.app, system.admin.login and cms.expert

The site is configured like this:

This error is given when user without administrator role is trying to change site config (pencil icon in the list of applications -> change properties in the modal dialog) and then save the content. If user changed site config, then changed a part and clicked “Apply” this will attempt to save the entire content and he will get an error.