The role of mucus secretion in the harvesting of symbionts during colonization of a squid light organ

NYHOLM, SV; DEPLANCKE, B; GASKINS, HR; APICELLA, M; MCFALL-NGAI, MJ: The role of mucus secretion in the harvesting of symbionts during colonization of a squid light organ

The Hawaiian bobtail squid Euprymna scolopes is colonized each generation by the bioluminescent bacterium Vibrio fischeri. During colonization, host-derived ciliary currents and mucus secretions aggregate Gram-negative bacteria outside the host�s light organ. Lectin staining and mucin histochemistry revealed that, at hatching, ciliated cells on the surface of the light organ contain dense neutral mucin stores. Within 2 h after exposure to Gram-negative or Gram-positive bacteria, these ciliated cells shed mucus that contributes to the formation of the bacterial aggregates. Exposure of freshly hatched squid to peptidoglycan, a membrane component common to Gram-negative and Gram-positive bacteria, led to host mucus secretion. However, only Gram-negative bacteria were able to form dense aggregates. At 48 h after successful colonization with V. fischeri, the host no longer aggregated bacteria and no shedding of host mucus was detected by lectin staining. This cessation of aggregation and mucus secretion was reversible upon curing the light organs of 48-h symbiotic animals with antibiotics. However, mucus secretion and bacterial aggregation were observed in uncolonized squid up to 120 h after hatching. Taken together, these data suggest that peptidoglycan is the responsible agent for inducing host mucus secretions. However, specific interactions with the bacterial symbiont V. fischeri are required to inhibit continued host mucus shedding and subsequent bacterial aggregation once a symbiosis has been established. Supported by NIH RR12294 and NSF IBN 9904601 to MMN and E. G. Ruby.

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