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Development, Vol 120, Issue 7 1719-1729, Copyright © 1994 by Company of Biologists
JOURNAL ARTICLES |
MK Montgomery and M McFall-Ngai
Department of Biological Sciences, University of Southern California, Los Angeles 90089-0371.
The mutualistic association between the squid Euprymna scolopes and the bacterium Vibrio fischeri is an emerging experimental system for the study of the influence of bacteria on animal development. Taking advantage of the ability to raise both this host and its microbial partner independently under laboratory conditions, we describe the effects of bacterial interactions on morphogenesis of the juvenile host symbiotic organ. Our results show that bacteria are essential for normal postembryonic development of the symbiotic organ, which involves changes in both the surface epithelium and the epithelial tissue within the organ where the bacterial culture will take up residence. Cell death induced by exposure to symbiotic V. fischeri results in the regression of a complex ciliated surface epithelium, a tissue that apparently functions to facilitate inoculation of the juvenile organ with the appropriate specific bacterial species. Regression of this tissue begins within hours of exposure to symbiosis-competent bacteria and progresses over the next 5 days, at which time full regression is complete, resulting in a symbiotic organ whose epithelial surface resembles that of the fully mature organ. Moreover, symbiosis-competent bacteria induce modification of the epithelial cells of the crypts that will house these symbionts; these cells undergo significant changes in shape and size in response to interactions with symbiotic V. fischeri. In contrast, we find that when these tissues are not exposed to the proper bacterial symbionts they remain in a state of arrested morphogenesis, a condition that can be rescued by interactions with symbionts. The results of these studies are the first experimental data demonstrating that a specific bacterial symbiont can play an inductive role in animal development.
This article has been cited by other articles:
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  D. M. Adin, N. J. Phillips, B. W. Gibson, M. A. Apicella, E. G. Ruby, M. J. McFall-Ngai, D. B. Hall, and E. V. Stabb Characterization of htrB and msbB Mutants of the Light Organ Symbiont Vibrio fischeri Appl. Envir. Microbiol., February 1, 2008; 74(3): 633 - 644. [Abstract] [Full Text] [PDF]
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 T. A. Koropatnick, J. R. Kimbell, and M. J. McFall-Ngai Responses of Host Hemocytes During the Initiation of the Squid-Vibrio Symbiosis Biol. Bull., February 1, 2007; 212(1): 29 - 39. [Abstract] [Full Text] [PDF]
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M. S. Goodson, M. Kojadinovic, J. V. Troll, T. E. Scheetz, T. L. Casavant, M. B. Soares, and M. J. McFall-Ngai Identifying Components of the NF-{kappa}B Pathway in the Beneficial Euprymna scolopes-Vibrio fischeri Light Organ Symbiosis Appl. Envir. Microbiol., November 1, 2005; 71(11): 6934 - 6946. [Abstract] [Full Text] [PDF]
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J. R. Kimbell and M. J. McFall-Ngai Symbiont-Induced Changes in Host Actin during the Onset of a Beneficial Animal-Bacterial Association Appl. Envir. Microbiol., March 1, 2004; 70(3): 1434 - 1441. [Abstract] [Full Text] [PDF]
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J. McCann, E. V. Stabb, D. S. Millikan, and E. G. Ruby Population Dynamics of Vibrio fischeri during Infection of Euprymna scolopes Appl. Envir. Microbiol., October 1, 2003; 69(10): 5928 - 5934. [Abstract] [Full Text] [PDF]
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S. V. Nyholm and M. J. McFall-Ngai Dominance of Vibrio fischeri in Secreted Mucus outside the Light Organ of Euprymna scolopes: the First Site of Symbiont Specificity Appl. Envir. Microbiol., July 1, 2003; 69(7): 3932 - 3937. [Abstract] [Full Text] [PDF]
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 D. S. Millikan and E. G. Ruby FlrA, a {sigma}54-Dependent Transcriptional Activator in Vibrio fischeri, Is Required for Motility and Symbiotic Light-Organ Colonization J. Bacteriol., June 15, 2003; 185(12): 3547 - 3557. [Abstract] [Full Text] [PDF]
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 J. R. Kimbell and M. J. McFall-Ngai The Squid-Vibrio Symbioses: From Demes to Genes Integr. Comp. Biol., April 1, 2003; 43(2): 254 - 260. [Abstract] [Full Text] [PDF]
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 S. F. Gilbert The Genome in Its Ecological Context: Philosophical Perspectives on Interspecies Epigenesis Ann. N.Y. Acad. Sci., December 1, 2002; 981(1): 202 - 218. [Abstract] [Full Text] [PDF]
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S. V. Nyholm, B. Deplancke, H. R. Gaskins, M. A. Apicella, and M. J. McFall-Ngai Roles of Vibrio fischeri and Nonsymbiotic Bacteria in the Dynamics of Mucus Secretion during Symbiont Colonization of the Euprymna scolopes Light Organ Appl. Envir. Microbiol., October 1, 2002; 68(10): 5113 - 5122. [Abstract] [Full Text] [PDF]
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C. R. DeLoney, T. M. Bartley, and K. L. Visick Role for Phosphoglucomutase in Vibrio fischeri-Euprymna scolopes Symbiosis J. Bacteriol., September 15, 2002; 184(18): 5121 - 5129. [Abstract] [Full Text] [PDF]
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J. Doino Lemus and M. J. McFall-Ngai Alterations in the Proteome of the Euprymna scolopes Light Organ in Response to Symbiotic Vibrio fischeri Appl. Envir. Microbiol., September 1, 2000; 66(9): 4091 - 4097. [Abstract] [Full Text]
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 S. V. Nyholm, E. V. Stabb, E. G. Ruby, and M. J. McFall-Ngai From the Cover: Establishment of an animal-bacterial association: Recruiting symbiotic vibrios from the environment PNAS, August 29, 2000; 97(18): 10231 - 10235. [Abstract] [Full Text] [PDF]
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K. L. Visick, J. Foster, J. Doino, M. McFall-Ngai, and E. G. Ruby Vibrio fischeri lux Genes Play an Important Role in Colonization and Development of the Host Light Organ J. Bacteriol., August 15, 2000; 182(16): 4578 - 4586. [Abstract] [Full Text]
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K. L. Visick and M. J. McFall-Ngai An Exclusive Contract: Specificity in the Vibrio fischeri-Euprymna scolopes Partnership J. Bacteriol., April 1, 2000; 182(7): 1779 - 1787. [Full Text]
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E. G. Ruby and K.-H. Lee The Vibrio fischeri-Euprymna scolopes Light Organ Association: Current Ecological Paradigms Appl. Envir. Microbiol., March 1, 1998; 64(3): 805 - 812. [Full Text]
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 L. H. Lamarcq and M. J. McFall-Ngai Induction of a Gradual, Reversible Morphogenesis of Its Host's Epithelial Brush Border by Vibrio fischeri Infect. Immun., February 1, 1998; 66(2): 777 - 785. [Abstract] [Full Text] [PDF]
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V. M. Weis, A. L. Small, and M. J. McFall-Ngai A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism PNAS, November 26, 1996; 93(24): 13683 - 13688. [Abstract] [Full Text] [PDF]
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