Collaborative Research: Structure and function: How microenvironment facilitates antimicrobial response to environmental stress in a defensive symbiosis

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Some animals form relationships with beneficial microbes that produce compounds that can inhibit pathogens and protect the host from disease. These beneficial microbes (or symbionts) are often critical for the animals and can influence the health of whole species and ecosystems. Animals that lay their eggs in the environment are at a particularly high risk from pathogens infecting these eggs and killing developing embryos. Therefore, some animals rely on beneficial symbionts that produce potent antimicrobial compounds to protect their eggs. However, we lack an understanding of how physical, biological, and chemical factors in eggs contribute to this protection that ultimately may stave off stresses such as pathogens and climate change. The Hawaiian bobtail squid has served as a model animal to study beneficial relationships with bacteria. This work will combine the expertise of a multidisciplinary team in microbiology, chemistry, and natural products research to test the hypothesis that the microenvironment of bobtail squid eggs helps beneficial bacteria produce effective antimicrobial compounds that defend against pathogenic microbes. Understanding these protective mechanisms will reveal how beneficial bacteria protect animals from environmental stress and may lead to new drug discoveries that can benefit humans. The research team will also create a new program that will cross-train the next generation of researchers in both chemistry, microbiology, and effective scientific communication to help our country prepare leaders for the bioeconomy.Many associations between hosts and symbionts are mediated via the production of specialized metabolites and other defensive compounds. Although great strides have been made in characterizing the microbial diversity of host-associated microbiota, how hosts and symbionts work together to achieve robust functional symbioses and their response to environmental stress is not well understood. This work will use a suite of multidisciplinary tools to understand how physical, chemical, and biological parameters interface with the environment to govern specialized metabolite production in a defensive symbiosis. The investigators will (I) determine how the egg microenvironment of the Hawaiian bobtail squid, Euprymna scolopes, contributes to antimicrobial production and localization, (II) determine how temperature influences antimicrobial response to fungal pathogens in ovum, and (III) characterize symbiont metabolite production using simplified ex vivo experiments to better understand in ovum defensive function. They will target known and new antimicrobial metabolites for expression analyses and localization ex vivo and in ovum. Broader implications of this research include transformative understanding of how host-microbe associations respond to threats of increasing global temperatures and concomitant pathogen stress. The team will integrate research and education by creating a new program, Chemistry of Squid Symbiosis (CheSS), that will cross-train students in symbiosis and natural product chemistry. The research team will also engage with the Skype-A-Scientist program to receive training on effective scientific communication and public outreach.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.