Literature DB >> 7924980

Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes.

M K Montgomery1, M McFall-Ngai.   

Abstract

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.

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Year:  1994        PMID: 7924980     DOI: 10.1242/dev.120.7.1719

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  72 in total

Review 1.  An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership.

Authors:  K L Visick; M J McFall-Ngai
Journal:  J Bacteriol       Date:  2000-04       Impact factor: 3.490

2.  Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association.

Authors:  Jennifer R Kimbell; Margaret J McFall-Ngai
Journal:  Appl Environ Microbiol       Date:  2004-03       Impact factor: 4.792

3.  Shedding light on bioluminescence regulation in Vibrio fischeri.

Authors:  Tim Miyashiro; Edward G Ruby
Journal:  Mol Microbiol       Date:  2012-05-02       Impact factor: 3.501

4.  THE EVOLUTIONARY ECOLOGY OF A SEPIOLID SQUID-VIBRIO ASSOCIATION: FROM CELL TO ENVIRONMENT.

Authors:  S V Nyholm; M K Nishiguchi
Journal:  Vie Milieu       Date:  2008       Impact factor: 0.236

5.  Phylogeographical patterns among Mediterranean sepiolid squids and their Vibrio symbionts: environment drives specificity among sympatric species.

Authors:  D J Zamborsky; M K Nishiguchi
Journal:  Appl Environ Microbiol       Date:  2010-11-12       Impact factor: 4.792

Review 6.  Animal-microbe interactions and the evolution of nervous systems.

Authors:  Heather L Eisthen; Kevin R Theis
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-01-05       Impact factor: 6.237

7.  Mutations in ampG and lytic transglycosylase genes affect the net release of peptidoglycan monomers from Vibrio fischeri.

Authors:  Dawn M Adin; Jacquelyn T Engle; William E Goldman; Margaret J McFall-Ngai; Eric V Stabb
Journal:  J Bacteriol       Date:  2008-12-12       Impact factor: 3.490

8.  Role of Major Toxin Virulence Factors in Pertussis Infection and Disease Pathogenesis.

Authors:  Karen Scanlon; Ciaran Skerry; Nicholas Carbonetti
Journal:  Adv Exp Med Biol       Date:  2019       Impact factor: 2.622

9.  Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity.

Authors:  Spencer V Nyholm; Margaret J McFall-Ngai
Journal:  Appl Environ Microbiol       Date:  2003-07       Impact factor: 4.792

Review 10.  Common trends in mutualism revealed by model associations between invertebrates and bacteria.

Authors:  John Chaston; Heidi Goodrich-Blair
Journal:  FEMS Microbiol Rev       Date:  2010-01       Impact factor: 16.408

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