Shaping the microenvironment: evidence for the influence of a host galaxin on symbiont acquisition and maintenance in the squid-vibrio symbiosis

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SummaryMost bacterial species make transitions between habitats, such as switching from free living to symbiotic niches. We provide evidence that a galaxin protein, EsGal1, of the squidEuprymna scolopesparticipates in both: (i) selection of the specific partnerVibrio fischerifrom the bacterioplankton during symbiosis onset and, (ii) modulation ofV. fischerigrowth in symbiotic maintenance. We identified two galaxins in transcriptomic databases and showed by quantitative reverse-transcriptase polymerase chain reaction that one (esgal1) was dominant in the light organ. Further,esgal1expression was upregulated by symbiosis, a response that was partially achieved with exposure to symbiont cell-envelope molecules. Confocal immunocytochemistry of juvenile animals localized EsGal1 to the apical surfaces of light-organ epithelia and surrounding mucus, the environment in whichV. fischericells aggregate before migration into the organ. Growth assays revealed that one repeat of EsGal1 arrested growth of Gram-positive bacterial cells, which represent the cell type first ‘winnowed’ during initial selection of the symbiont. The EsGal1-derived peptide also significantly decreased the growth rate ofV. fischeriin culture. Further, when animals were exposed to an anti-EsGal1 antibody, symbiont population growth was significantly increased. These data provide a window into how hosts select symbionts from a rich environment and govern their growth in symbiosis.

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