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Applied and Environmental Microbiology, October 2002, p. 5113-5122, Vol. 68, No. 10
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.10.5113-5122.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Roles of Vibrio fischeri and Nonsymbiotic Bacteria in the Dynamics of Mucus Secretion during Symbiont Colonization of the Euprymna scolopes Light Organ

Spencer V. Nyholm,1,2,{dagger} Bart Deplancke,3 H. Rex Gaskins,3,4 Michael A. Apicella,5 and Margaret J. McFall-Ngai1*

Pacific Biomedical Research Center, Kewalo Marine Laboratory, University of Hawaii, Honolulu, Hawaii 96813,1 Department of Zoology, University of Hawaii at Manoa, Honolulu, Hawaii 96822,2 Division of Nutritional Sciences,3 Departments of Animal Sciences and Veterinary Pathobiology, University of Illinois, Urbana-Champaign, Illinois 61801,4 Department of Microbiology, University of Iowa, Iowa City, Iowa 522425

Received 20 March 2002/ Accepted 2 July 2002

During light organ colonization of the squid Euprymna scolopes by Vibrio fischeri, host-derived mucus provides a surface upon which environmental V. fischeri forms a biofilm and aggregates prior to colonization. In this study we defined the temporal and spatial characteristics of this process. Although permanent colonization is specific to certain strains of V. fischeri, confocal microscopy analyses revealed that light organ crypt spaces took up nonspecific bacteria and particles that were less than 2 µm in diameter during the first hour after hatching. However, within 2 h after inoculation, these cells or particles were not detectable, and further entry by nonspecific bacteria or particles appeared to be blocked. Exposure to environmental gram-negative or -positive bacteria or bacterial peptidoglycan caused the cells of the organ's superficial ciliated epithelium to release dense mucin stores at 1 to 2 h after hatching that were used to form the substrate upon which V. fischeri formed a biofilm and aggregated. Whereas the uncolonized organ surface continued to shed mucus, within 48 h of symbiont colonization mucus shedding ceased and the formation of bacterial aggregations was no longer observed. Eliminating the symbiont from the crypts with antibiotics restored the ability of the ciliated fields to secrete mucus and aggregate bacteria. While colonization by V. fischeri inhibited mucus secretion by the surface epithelium, secretion of host-derived mucus was induced in the crypt spaces. Together, these data indicate that although initiation of mucus secretion from the superficial epithelium is nonspecific, the inhibition of mucus secretion in these cells and the concomitant induction of secretion in the crypt cells are specific to natural colonization by V. fischeri.

* Corresponding author. Mailing address: Pacific Biomedical Research Center, Kewalo Marine Laboratory, 41 Ahui Street, Honolulu, HI 96813. Phone: (808) 539-7310. Fax: (808) 599-4817. E-mail: mcfallng{at}hawaii.edu.

{dagger} Present address: Stanford University, Hopkins Marine Station, Pacific Grove, CA 93950.

Applied and Environmental Microbiology, October 2002, p. 5113-5122, Vol. 68, No. 10
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.10.5113-5122.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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