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  • Review Article
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The winnowing: establishing the squid–vibrio symbiosis

Nature Reviews Microbiology volume 2, pages 632–642 (2004)Cite this article

Key Points

  • Symbiotic interactions that involve microorganisms are widespread, but just how the host and the microorganism come to co-exist is not well understood. The mechanisms that underlie this process are fascinating and have implications for the host–pathogen relationship, as partner choice and pathogen interactions might overlap. Here, the authors use the association between the Hawaiian bobtail squid Euprymna scolopes and the luminous bacterium Vibrio fischeri — studied for more then 15 years — to illustrate the beauty and complexity of horizontally (environmentally) transmitted symbiotic associations.

  • Chance encounters do not precede symbiotic development: the authors review how the host enriches its local environment with the symbiont populations from which newly hatched juvenile hosts will become colonized.

  • After the initial encounter, which can be within a few seconds of the squid-egg hatching, the symbiont is selected from the plethora of microorganisms present, akin to sorting the wheat from the chaff. These processes are reviewed, and include the roles of ciliary currents and mucus in colonization of the nascent squid light organ.

  • Following establishment of the association, Vibrio fischeri induces a series of developmental changes which help transform the host's light organ from one poised to initiate symbiosis to a mature, functional light organ. The changes in the organ are described, together with some of the bacterial factors involved.

  • Host factors might include defence functions, which are activated on encountering a microorganism. The authors include a description of what is known about squid immune functions and the bacterial mutants that have been studied in an attempt to dissect the colonization process. Bacterial phenotypes that affect colonization include motility, oxidative stress defences and lipid synthesis.

  • Finally, the exciting impact of genomics on this partnership is discussed: not only is the Vibrio fischeri genome now complete, an extensive squid EST collection is available. Data mining, together with microarrays, will further our understanding of how this exclusive partnership is established and maintained.

Abstract

Most symbiotic associations between animals and microorganisms are horizontally transmitted — the microorganisms are acquired from the environment by each generation of the host. How are exclusive partnerships established in the context of the thousands of other microbial species that are present in the environment? Similar to winnowing during a harvest, the symbiosis between the squid Euprymna scolopes and its luminous bacterial symbiont Vibrio fischeri involves a step-wise elimination of potential interlopers that ensures separation of the 'grain' from the 'chaff'.

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Figure 1: The diel pattern of host behaviour and the associated fluctuations in symbiont population density in the light organ.
Figure 2: The juvenile light-organ system.
Figure 3: The initial interactions of the juvenile host with the environment.
Figure 4: The harvesting of the specific symbiont: mucus secretion, aggregation, dominance and migration.
Figure 5: The gradual, symbiont-induced regression of the ciliated epithelium of the juvenile light organ.
Figure 6: Timeline showing early events and signals during the onset of symbiosis.
Figure 7: Initiation, accommodation and persistence mutants of Vibrio fischeri.
Figure 8: The winnowing.

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References

  1. McFall-Ngai, M. J. & Ruby, E. G. Symbiont recognition and subsequent morphogenesis as early events in an animal–bacterial symbiosis. Science 254, 1491–1494 (1991).

    Article  CAS  Google Scholar 

  2. McFall-Ngai, M. J. & Ruby, E. G. Squids and vibrios: when they first meet. BioScience 48, 257–265 (1998).

    Article  Google Scholar 

  3. McFall-Ngai, M. J. Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242, 1–14 (2002). Discusses the influence of bacteria on invertebrate and vertebrate host development.

    Article  CAS  Google Scholar 

  4. Jones, B. W. & Nishiguchi, M. K. Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar. Biol. 144, 1151–1155 (2004).

    Article  Google Scholar 

  5. Ruby, E. G. Lessons from a cooperative bacterial–animal association: the Vibrio fischeri–Euprymna scolopes light organ symbiosis. Annu. Rev. Microbiol. 50, 591–624 (1996).

    Article  CAS  Google Scholar 

  6. Haygood, M. G. Light organ symbioses in fishes. Crit. Rev. Microbiol. 19, 191–216 (1993).

    Article  CAS  Google Scholar 

  7. Gros, O., Darrasse, A., Durand, P., Frenkiel, L. & Moueza, M. Environmental transmission of a sulfur-oxidizing bacterial gill endosymbiont in the tropical lucinid bivalve Codakia orbicularis. Appl. Environ. Microbiol. 62, 2324–30 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Muller-Parker, G. & D'Elia, C. F. in Life and Death of Coral Reefs (ed. Birkeland, C.) 96–113 (Chapman and Hall, New York, 1997).

    Book  Google Scholar 

  9. Ruby, E. G. & Lee, K. H. The Vibrio fischeri–Euprymna scolopes light organ association: current ecological paradigms. Appl. Environ. Microbiol. 64, 805–812 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Lee, K. -H. & Ruby, E. G. Detection of the light organ symbiont, Vibrio fischeri, in Hawaiian seawater by using lux gene probes. Appl. Environ. Microbiol. 58, 942–947 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Lee, K. H. & Ruby, E. G. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl. Environ. Microbiol. 60, 1565–1571 (1994). Demonstrated that populations of the squid host dramatically influence the concentration of V. fischeri in the bacterioplankton, which in turn affects the efficiency with which juvenile squid are colonized at hatching.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Boettcher, K. J., Ruby, E. G. & McFall-Ngai, M. J. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J. Comp. Physiol. 179, 65–73 (1996).

    Article  Google Scholar 

  13. Nyholm, S. V. & McFall-Ngai, M. J. Sampling the microenvironment of the Euprymna scolopes light organ: description of a population of host cells with the bacterial symbiont Vibrio fischeri. Biol. Bull. 195, 89–97 (1998).

    Article  CAS  Google Scholar 

  14. Ruby, E. G. & Asato, L. M. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch. Microbiol. 159, 160–167 (1993).

    Article  CAS  Google Scholar 

  15. McCann, J., Stabb, E. V., Millikan, D. S. & Ruby, E. G. Population effects of Vibrio fischeri during infection of Euprymna scolopes. Appl. Environ. Microbiol. 69, 5928–5934 (2003).

    Article  CAS  Google Scholar 

  16. McFall-Ngai, M. J. & Ruby, E. G. Sepiolids and vibrios: when they first meet. BioScience 48, 257–265 (1998).

    Article  Google Scholar 

  17. Montgomery, M. K. & McFall-Ngai, M. J. The effect of bacterial symbionts on early post-embryonic development of a squid light organ. Development 120, 1719–1729 (1994).

    CAS  PubMed  Google Scholar 

  18. Nyholm, S. V., Stabb, E. V., Ruby, E. G. & McFall-Ngai, M. J. Establishment of an animal–bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl Acad. Sci. USA 97, 10231–10235 (2000). Provided the first mechanism by which an aquatic animal could harvest relatively scarce symbionts from the environment.

    Article  CAS  Google Scholar 

  19. Nyholm, S. V., Deplancke, B., Gaskins, H. R., Apicella, M. A. & McFall-Ngai, M. J. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68, 5113–5122 (2002).

    Article  CAS  Google Scholar 

  20. Nyholm, S. V. & McFall-Ngai, M. J. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69, 3932–3937 (2003).

    Article  CAS  Google Scholar 

  21. Deloney-Marino, C. R., Wolfe, A. J. & Visick K. L. Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl. Environ. Microbiol. 69, 7527–7530 (2003).

    Article  CAS  Google Scholar 

  22. Sonnenberg, J. L., Angenent, L. T. & Gordon, J. I. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nature Immunol. 5, 569–573 (2004). Reviews our knowledge of the microanatomical, molecular and biochemical interactions of beneficial intestinal bacteria and their mammalian hosts.

    Article  Google Scholar 

  23. Salyers, A. A., Pajeau, M. & McCarthy, R. E. Importance of mucopolysaccarides as substrates for Bacteroides thetaiotaomicron growing in intestinal tracts of exgermfree mice. Appl. Environ. Microbiol. 54, 1970–1976 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Hwa, V. & Salyers, A. A. Analysis of two chondroitin sulfate utilization mutants of Bacteroides thetaiotaomicron that differ in their abilities to compete with the wild type in the gastrointestinal tracts of germfree mice. Appl. Environ. Microbiol. 58, 869–876 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Davidson, S. K. & McFall-Ngai, M. J. NO means 'yes' in the squid–vibrio symbiosis: the role of nitric oxide in the initiation of a beneficial association. Cell. Microbiol. (in the press).

  26. Weis, V. M., Small, A. L. & McFall-Ngai, M. J. A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna–Vibrio mutualism. Proc. Natl Acad. Sci. USA 93, 13683–13688 (1996).

    Article  CAS  Google Scholar 

  27. Small, A. L. & McFall-Ngai, M. J. A halide peroxidase in tissues that interact with bacteria in the host squid Euprymna scolopes. J. Cell. Biochem. 72, 445–457 (1999).

    Article  CAS  Google Scholar 

  28. Koropatnick, T., Apicella, M. A. & McFall-Ngai, M. J. Symbiont-induced developmental remodeling of the Euprymna scolopes light organ involves microbial membrane factors and host hemocyte migration. Mol. Biol. Cell. 13, 252a (2002).

    Google Scholar 

  29. Kimbell, J. R. & McFall-Ngai, M. J. Symbiont-induced changes in host actin during the onset of a beneficial animal–bacterial association. Appl. Environ. Microbiol. 70, 1434–1441 (2004).

    Article  CAS  Google Scholar 

  30. Lamarcq, L. H. & McFall-Ngai, M. J. Induction of a gradual, reversible morphogenesis of its host's epithelial brush border by Vibrio fischeri. Infect. Immun. 66, 777–785 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Foster, J. S., Apicella, M. A. & McFall-Ngai, M. J. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev. Biol. 226, 242–254 (2000). Demonstrated that bacterial lipopolysaccharide induces apoptosis in a normal developmental programme of an animal–bacterial interaction, not only as part of the cytopathology of a bacterial infection.

    Article  CAS  Google Scholar 

  32. Kaufman, M. R., Ikeda, Y., Patton, C., Van Dykhuizen, G. & Epel, D. Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Biol. Bull. 194, 36–43 (1998).

    Article  CAS  Google Scholar 

  33. Southward, E. C. Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): implications for relationship between Vestimentifera and Pogonophora. J. Mar. Biolog. Assoc. UK 68, 465–487 (1988).

    Article  Google Scholar 

  34. Jensen, E. T., Kharazmi, A., Hoiby, N. & Costerton, J. W. Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa biofilms. APMIS 100, 727–733 (1992).

    Article  CAS  Google Scholar 

  35. Barbieri, J. T., Riese, M. J. & Aktories, K. Bacterial toxins that modify the actin cytoskeleton. Annu. Rev. Cell Dev. Biol. 18, 315–344 (2002).

    Article  CAS  Google Scholar 

  36. Fullner, K. J., Lencer, W. I. & Mekalanos, J. J. Vibrio cholerae-induced cellular responses of polarized T84 intestinal epithelial cells are dependent on production of cholera toxin and the RTX toxin. Infect. Immun. 69, 6310–6317 (2001).

    Article  CAS  Google Scholar 

  37. Doino, J. A. & McFall-Ngai, M. J. Transient exposure to competent bacteria initiates symbiosis-specific squid light organ morphogenesis. Biol. Bull. 189, 347–355 (1995).

    Article  CAS  Google Scholar 

  38. Ruby, E. G. The Euprymna scolopes–Vibrio fischeri symbiosis: a biomedical model for the study of bacterial colonization of animal tissue. J. Mol. Microbiol. Biotech. 1, 13–21 (1999). Compares the colonization determinants of pathogenic and beneficial vibrios, and outlines the genetic tools available in Vibrio fischeri.

    CAS  Google Scholar 

  39. Graf, J., Dunlap, P. V. & Ruby, E. G. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176, 6986–6991 (1994).

    Article  CAS  Google Scholar 

  40. Millikan, D. S. & Ruby, E. G. FlrA, a σ54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J. Bacteriol. 185, 3547–3557 (2003).

    Article  CAS  Google Scholar 

  41. Millikan, D. S. & Ruby, E. G. Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects. Appl. Environ. Microbiol. 68, 2519–2528 (2002).

    Article  CAS  Google Scholar 

  42. Aeckersberg, F., Lupp, C., Feliciano, B. & Ruby, E. G. Vibrio fischeri outer membrane protein OmpU plays a role in normal symbiotic colonization. J. Bacteriol. 183, 6590–6597 (2001).

    Article  CAS  Google Scholar 

  43. Whistler, C. A. & Ruby, E. G. GacA regulates symbiotic colonization traits of Vibrio fischeri and facilitates a beneficial association with an animal host. J. Bacteriol. 185, 7202–7212 (2003).

    Article  CAS  Google Scholar 

  44. Visick, K. L. & Skoufos, L. M. Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J. Bacteriol. 183, 835–842 (2001).

    Article  CAS  Google Scholar 

  45. Lupp, C., Urbanowski, M., Greenberg, E. P. & Ruby, E. G. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol. Microbiol. 50, 319–331 (2003).

    Article  CAS  Google Scholar 

  46. Fidopiastis, P. M., Miyamoto, C. M., Jobling, M. G., Meighen, E. A. & Ruby, E. G. LitR, a new transcriptional activator in Vibrio fischeri, regulates luminescence and symbiotic light organ colonization. Mol. Microbiol. 45, 131–143 (2002).

    Article  CAS  Google Scholar 

  47. Graf, J. & Ruby, E. G. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl Acad. Sci. USA 95, 1818–1822 (1998).

    Article  CAS  Google Scholar 

  48. Deloney, C. R., Bartley, T. M. & Visick, K. L. Role for phosphoglucomutase in Vibrio fischeri–Euprymna scolopes symbiosis. J. Bacteriol. 184, 5121–5129 (2002).

    Article  CAS  Google Scholar 

  49. Visick, K. L., Foster, J., Doino, J., McFall-Ngai, M. J. & Ruby, E. G. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182, 4578–4586 (2000). Showed that luminescence is required for persistence of the bacterial symbiont in the host squid light organ, a requirement that correlates with the ability of the symbiont to induce oedema in host cells with which it directly associates.

    Article  CAS  Google Scholar 

  50. Graf, J. & Ruby, E. G. Novel effects of a transposon insertion in the Vibrio fischeri glnD gene: defects in iron uptake and symbiotic persistence, as well as nitrogen utilization. Mol. Microbiol. 37, 168–179 (2000).

    Article  CAS  Google Scholar 

  51. Visick, K. L. & Ruby, E. G. The periplasmic, group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and approach to stationary phase. J. Bacteriol. 180, 2087–2092 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Nealson, K. H. & Hastings, J. W. Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43, 496–518 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Byrd, J. C., Yunker, C. K., Xu, Q. S., Sternberg, L. R. & Bresalier, R. S. Inhibition of gastric mucin synthesis by Helicobacter pylori. Gastroenterology 118, 1072–1079 (2000).

    Article  CAS  Google Scholar 

  54. Micots, I., Augeron, C., Laboisse, C. L., Muzeau, F. & Megraud, F. Mucin exocytosis: a major target for Helicobacter pylori. J. Clin. Pathol. 46, 241–245 (1993).

    Article  CAS  Google Scholar 

  55. Dinwiddle, R. Pathogenesis of lung disease in cystic fibrosis. Respiration 67, 3–8 (2000).

    Article  Google Scholar 

  56. Magor, B. G. & Magor, K. E. Evolution of effectors and receptors of innate immunity. Dev. Comp. Immunol. 25, 651–682 (2001).

    Article  CAS  Google Scholar 

  57. Nonaka, M. & Yoshizaki, F. Evolution of the complement system. Mol. Immunol. 40, 897–902 (2004).

    Article  CAS  Google Scholar 

  58. Azumi, K. et al. Genomic analysis of immunity in a Urochordate and emergence of the vertebrate immune system: 'waiting for Godot'. Immunogenetics 55, 570–581 (2003).

    Article  CAS  Google Scholar 

  59. Douglas, A. E. Symbiotic Interactions (Oxford Science Publications, Oxford, 1994).

    Google Scholar 

  60. Friedrich, A. B. et al. Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar. Biol. 134, 461–470 (1999).

    Article  Google Scholar 

  61. Benayahu, Y. & Schleyer, M. H. Reproduction in Anthelia glauca (Octocorallia: Xeniidae): transmission of algal symbionts during planular brooding. Mar. Biol. 131, 433–442 (1998).

    Article  Google Scholar 

  62. Schwartz, D. A., Krupp, D. A. & Weis, V. M. Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol. Bull. 196, 70–79 (1999).

    Article  Google Scholar 

  63. Harrison, P. L. & Wallace, C. C. Reproduction, dispersal and recruitment of scleractinian corals (Elsevier, Amsterdam, 1990).

    Google Scholar 

  64. Loh, W. K. H., Loi, T., Carter, D. & Hoegh-Guldberg, O. Genetic variability of the symbiotic dinoflagellates from the wide-ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar. Ecol. Prog. Ser. 222, 97–107 (2001).

    Article  Google Scholar 

  65. Cary, S. C., Warren, W., Anderson, E. & Giovannoni, S. J. Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont-specific polymerase chain reaction amplification and in situ hybridization techniques. Mol. Mar. Biol. Biotechnol. 2, 51–62 (1993).

    CAS  PubMed  Google Scholar 

  66. Cary, S. C. & Giovannoni, S. J. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl Acad. Sci. USA 90, 5695–5699 (1993).

    Article  CAS  Google Scholar 

  67. Distel, D. L. et al. Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J. Bacteriol. 170, 2506–2510 (1988).

    Article  CAS  Google Scholar 

  68. Won, Y. J. et al. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl. Environ. Microbiol. 69, 6785–6792 (2003).

    Article  CAS  Google Scholar 

  69. McFall-Ngai, M. J. Consequences of evolving with bacterial symbionts: insights from the squid–vibrio associations. Annu. Rev. Ecol. Syst. 30, 235–256 (1999).

    Article  Google Scholar 

  70. Grigioni, S., Boucher-Rodoni, R., Demarta, A., Tonolla, M. & Peduzzi, R. Phylogenetic characterization of bacterial symbionts in the accessory nidamental gland of the sepiolid Sepia officnialis Cephalopoda:Decapoda. Mar. Biol. 136, 217–222 (2000).

    Article  CAS  Google Scholar 

  71. Barbieri, E. et al. Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo peali (Cephalopoda: Loliginidae). Environ. Microbiol. 3, 151–167 (2001).

    Article  CAS  Google Scholar 

  72. Baumann, P., Moran, N. A. & Baumann, L. The evolution and genetics of aphid endosymbionts. BioScience 47, 12–20 (1997).

    Article  Google Scholar 

  73. O'Neil, S. L., Hoffmann, A. A. & Werren, J. H. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (Oxford University Press, New York, 1997).

    Google Scholar 

  74. Zimmer, C. Wolbachia: a tale of sex and survival. Science 292, 1093–1095 (2001).

    Article  CAS  Google Scholar 

  75. Abe, T., Bignell, D. E. & Higashi, M. Termites: Evolution, Sociality, Symbiosis, Ecology (Kluwer Academic, Massachusetts, 2000).

    Book  Google Scholar 

  76. Hooper, L. V. et al. Molecular analysis of commensal host–microbial relationships in the intestine. Science 291, 881–884 (2001).

    Article  CAS  Google Scholar 

  77. Russell, J. B. & Rychlik, J. L. Factors that alter rumen ecology. Science 292, 1119–1122 (2001).

    Article  CAS  Google Scholar 

  78. Hooper, L. V. & Gordon, J. I. Commensal host–bacterial relationships in the gut. Science 292, 1115–1118 (2001).

    Article  CAS  Google Scholar 

  79. Paster, B. et al. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770–3783 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank E. G. Ruby for helpful comments on the manuscript. Work on the squid–Vibrio system is funded by the National Science Foundation, the National Institutes of Health and the W. M. Keck Foundation.

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Authors and Affiliations

  1. Department of Pathology, Stanford University, School of Medicine, Palo Alto, 94305, California, USA

    Spencer V. Nyholm

  2. Hopkins Marine Station, Pacific Grove, 93950, California, USA

    Spencer V. Nyholm

  3. Department of Medical Microbiology and Immunology, 1300 University Avenue, University of Wisconsin School of Medicine, Madison, 53706-1532, Wisconsin, USA

    Margaret McFall-Ngai

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Correspondence to Margaret McFall-Ngai.

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FURTHER INFORMATION

V. fischeri genome

E. scolopes EST database

Margaret McFall-Ngai's laboratory

Glossary

STOCHASTICALLY

Random interactions that are not predetermined.

CHECKPOINT

A hurdle imposed by the host that confers greater specificity to the symbiont during colonization.

ACCOMMODATION MUTANTS

Mutants of Vibrio fischeri that colonize the light organ of the host at lower numbers than wild-type symbionts.

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Nyholm, S., McFall-Ngai, M. The winnowing: establishing the squid–vibrio symbiosis. Nat Rev Microbiol 2, 632–642 (2004). https://doi.org/10.1038/nrmicro957

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