Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes - PubMed (original) (raw)
. 1994 Jul;120(7):1719-29.
doi: 10.1242/dev.120.7.1719.
Affiliations
- PMID: 7924980
- DOI: 10.1242/dev.120.7.1719
Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes
M K Montgomery et al. Development. 1994 Jul.
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.
Similar articles
- Persistent Interactions with Bacterial Symbionts Direct Mature-Host Cell Morphology and Gene Expression in the Squid-Vibrio Symbiosis.
Kremer N, Koch EJ, El Filali A, Zhou L, Heath-Heckman EAC, Ruby EG, McFall-Ngai MJ. Kremer N, et al. mSystems. 2018 Oct 2;3(5):e00165-18. doi: 10.1128/mSystems.00165-18. eCollection 2018 Sep-Oct. mSystems. 2018. PMID: 30320217 Free PMC article. - Late postembryonic development of the symbiotic light organ of Euprymna scolopes (Cephalopoda: Sepiolidae).
Montgomery MK, McFall-Ngai MJ. Montgomery MK, et al. Biol Bull. 1998 Dec;195(3):326-36. doi: 10.2307/1543144. Biol Bull. 1998. PMID: 9924775 - Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis.
Ruby EG. Ruby EG. Annu Rev Microbiol. 1996;50:591-624. doi: 10.1146/annurev.micro.50.1.591. Annu Rev Microbiol. 1996. PMID: 8905092 Review. - Nocturnal Acidification: A Coordinating Cue in the _Euprymna scolopes_-Vibrio fischeri Symbiosis.
Pipes BL, Nishiguchi MK. Pipes BL, et al. Int J Mol Sci. 2022 Mar 29;23(7):3743. doi: 10.3390/ijms23073743. Int J Mol Sci. 2022. PMID: 35409100 Free PMC article. Review.
Cited by
- Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host.
Verma SC, Miyashiro T. Verma SC, et al. Appl Environ Microbiol. 2016 Sep 16;82(19):5990-6. doi: 10.1128/AEM.01770-16. Print 2016 Oct 1. Appl Environ Microbiol. 2016. PMID: 27474717 Free PMC article. - THE EVOLUTIONARY ECOLOGY OF A SEPIOLID SQUID-VIBRIO ASSOCIATION: FROM CELL TO ENVIRONMENT.
Nyholm SV, Nishiguchi MK. Nyholm SV, et al. Vie Milieu. 2008;58(2):175-184. Vie Milieu. 2008. PMID: 20414482 Free PMC article. - The Vibrio fischeri-Euprymna scolopes Light Organ Association: Current Ecological Paradigms.
Ruby EG, Lee KH. Ruby EG, et al. Appl Environ Microbiol. 1998 Mar;64(3):805-12. doi: 10.1128/AEM.64.3.805-812.1998. Appl Environ Microbiol. 1998. PMID: 16349524 Free PMC article. No abstract available. - A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide.
Brennan CA, Hunt JR, Kremer N, Krasity BC, Apicella MA, McFall-Ngai MJ, Ruby EG. Brennan CA, et al. Elife. 2014 Mar 4;3:e01579. doi: 10.7554/eLife.01579. Elife. 2014. PMID: 24596150 Free PMC article. - A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism.
Weis VM, Small AL, McFall-Ngai MJ. Weis VM, et al. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13683-8. doi: 10.1073/pnas.93.24.13683. Proc Natl Acad Sci U S A. 1996. PMID: 8942994 Free PMC article.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources