Abstract Associations with pathogenic bacteria have
recently been shown to initiate apoptotic programs in the
cells of their animal hosts, where host cell death is hypothesized
to be a response of the immune system, either
initiated as a mechanism of host defense or bacterial offense.
In this study, we present evidence that bacterial
initiation of apoptosis is neither restricted to pathogenesis
nor to the initation of an immune response. In the cooperative
association between the sepiolid squid Euprymna
scolopes and the luminous bacterium Vibrio fischeri,
the bacteria induce a dramatic morphogenesis of
the host tissues during the first few days of interaction
between these partners. The most striking change is the
bacteria-triggered loss of an extensive superficial epithelium
that potentiates the infection process. Our analyses
of these tissues revealed that the bacteria induce apoptosis
in the cells that comprise this epithelium within hours
of the interaction with bacteria. Ultrastructural analysis
revealed that after 24 h the integrity of the epithelium
had been lost, i.e., the basement membrane had degenerated
and the majority of the cells exhibited signs of apoptosis,
most notably chromatin condensation. Analysis
of these tissues with probes that reveal intracellular acidification
showed that the cells first undergo an initial acidification
beginning about 6–8 h after exposure to V. fischeri.
As determined by end-labeling of DNA fragments,
extensive endonuclease activity was detected at
approximately 16–20 h post-infection. These data provide
evidence that cooperative bacteria can participate in
the remodeling of host tissues through the induction of
host apoptotic programs.