Actually the log SAWarning: Object of type <Update> not in session, add operation along 'User.updates' will not proceed (This warning originated from the Session 'autoflush' process, which was invoked automatically in response to a user-initiated operation.) makes me particularly suspicious of SQLAlchemy.

The way the process used to work (from my hazy memory) was when a request came in, before the handler ran middleware opened a new SQLAlchemy session and somehow ensured the handler used it, and then the session got closed and committed after the request handler returned in the post-request middleware. This sounds like during the request handler the operations aren't happening in that session at all, or the session already got closed somehow. "autoflush" sounds like a likely candidate.

This is what I've seen elsewhere:

[2024-12-13 10:36:42,990 twisted INFO] Log opened.
Exception in thread CrochetReactor:
[2024-12-13 10:36:42,991 twisted INFO] Log opened.
Traceback (most recent call last):
  File "/usr/lib64/python3.13/threading.py", line 1041, in _bootstrap_inner
    self.run()
    ~~~~~~~~^^
  File "/usr/lib64/python3.13/threading.py", line 992, in run
    self._target(*self._args, **self._kwargs)
    ~~~~~~~~~~~~^^^^^^^^^^^^^^^^^^^^^^^^^^^^^
  File "/srv/image-uploader/venv/lib64/python3.13/site-packages/crochet/_eventloop.py", line 360, in <lambda>
    target=lambda: self._reactor.run(installSignalHandlers=False),
                   ~~~~~~~~~~~~~~~~~^^^^^^^^^^^^^^^^^^^^^^^^^^^^^
  File "/srv/image-uploader/venv/lib64/python3.13/site-packages/twisted/internet/asyncioreactor.py", line 252, in run
    self.startRunning(installSignalHandlers=installSignalHandlers)
    ~~~~~~~~~~~~~~~~~^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^
  File "/srv/image-uploader/venv/lib64/python3.13/site-packages/twisted/internet/base.py", line 924, in startRunning
    raise error.ReactorAlreadyRunning()
twisted.internet.error.ReactorAlreadyRunning