What happens if my city has 3 religions, does it benefit from all of the follower beliefs, or does it just work for the current most dominant religion?
It only gets the benefit from the current most-dominant religion in the city. The rest of the religions in your cities are, obviously, heretics and infidels. (Just ask the dominant religion!)
I've seen this in the Into The Renaissance scenario, where the Catholics can buy troops with faith; you can't buy troops unless Catholicism is the dominant religion.
As of the Brave New World expansion, there is now a policy in the Piety culture tree to grant the Pantheon bonus of the second-most-popular religion in your cities. Pantheon bonuses are pretty small, but it is something from a non-dominant religion in your city.