The winnowing: establishing the squid–vibrio symbiosis

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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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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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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