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Breaking the language barrier: experimental evolution of non-native Vibrio fischeri in squid tailors luminescence to the host

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Abstract

Although most Vibrio fischeri isolates are capable of symbiosis, the coevolution of certain strains with the Hawaiian bobtail squid, Euprymna scolopes, has led to specific adaptation to this partnership. For instance, strains from different hosts or from a planktonic environment are ineffective squid colonists. Even though bioluminescence is a symbiotic requirement, curiously, symbionts of E. scolopes are dim in culture relative to fish symbionts and free-living isolates. It is unclear whether this dim phenotype is related to the symbiosis or simply coincidental. To further explore the basis of symbiont specificity, we developed an experimental evolution model that utilizes the daily light organ venting behavior of the squid and horizontal acquisition of symbionts for serial passage of cultures. We passaged six populations each derived from the squid-naïve strains of V. fischeri MJ11 (a fish symbiont) and WH1 (a free-living isolate) through a series of juvenile squid light organs. After 15 serially colonized squid for each population, or an estimated 290–360 bacterial generations, we isolated representatives of the light organ populations and characterized their bioluminescence. Multiple evolved lines of both strains produced significantly less bioluminescence both in vitro and in vivo. This reduction in bioluminescence did not correlate with reduced quorum sensing for most isolates tested. The remarkable phenotypic convergence with squid symbionts further emphasizes the importance of bioluminescence in this symbiosis, and suggests that reduced light production is a specific adaptation to the squid.

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Acknowledgments

We thank Randi Desy, Anna Tyzik, and Rachel Donner for their assistance with culture evolution and in characterizing phenotypes of evolved strains, and Jenny Mahoney, Alicia Ballok, Michael Wollenberg, Karen Visick, and Spencer Nyholm for their helpful discussions on experimental design and analysis. This work was supported by a developmental grant from the New Hampshire Agricultural Experimentation Station NH00520 Hatch.

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Authors and Affiliations

  1. Graduate Program in Microbiology, University of New Hampshire, 46 College Rd., Durham, NH, 03824, USA

    Brian M. Schuster, Lauren A. Perry, Vaughn S. Cooper & Cheryl A. Whistler

  2. Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, 46 College Rd., Durham, NH, 03824, USA

    Vaughn S. Cooper & Cheryl A. Whistler

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  1. Brian M. Schuster
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  2. Lauren A. Perry
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  4. Cheryl A. Whistler
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Correspondence to Cheryl A. Whistler.

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Schuster, B.M., Perry, L.A., Cooper, V.S. et al. Breaking the language barrier: experimental evolution of non-native Vibrio fischeri in squid tailors luminescence to the host. Symbiosis 51, 85–96 (2010). https://doi.org/10.1007/s13199-010-0074-2

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