Margaret J. McFall-Ngai

The establishment of a productive symbiosis between Euprymna scolopes , the Hawaiian bobtail squid, and its luminous bacterial symbiont, Vibrio fischeri , is mediated by transcriptional changes in both partners. A key challenge to unraveling the steps required to successfully initiate this and many other symbiotic associations is characterization of the timing and location of these changes. We report on the adaptation of hybridization chain reaction-fluorescent in situ hybridization (HCR-FISH) to simultaneously probe the spatiotemporal regulation of targeted genes in both E. scolopes and V. fischeri . This method revealed localized, transcriptionally coregulated epithelial cells within the light organ that responded directly to the presence of bacterial cells while, at the same time, provided a sensitive means to directly show regulated gene expression within the symbiont population. Thus, HCR-FISH provides a new approach for characterizing habitat transition in bacteria and for discovering host tissue responses to colonization.

The new technology of next-generation sequencing is changing our perceptions of the form and function of the biological world. The emerging data reveal an array of microbes that is more vast and more central to all biological processes than previously appreciated. Further, evidence is accumulating that the alliances of microbes with one another and with constituents of the macrobiological world are critical for the health of the biosphere. This contribution summarizes the basic arguments as to why, when considering the biochemical adaptations of animals, we should integrate the roles of their microbial partners.

Developmental biology is among the many subdisciplines of the life sciences being transformed by our increasing awareness of the role of coevolved microbial symbionts in health and disease. Most symbioses are horizontally acquired, i.e., they begin anew each generation. In such associations, the embryonic period prepares the animal to engage with the coevolved partner(s) with fidelity following birth or hatching. Once interactions are underway, the microbial partners drive maturation of tissues that are either directly associated with or distant from the symbiont populations. Animal alliances often involve complex microbial communities, such as those in the vertebrate gastrointestinal tract. A series of simpler-model systems is providing insight into the basic rules and principles that govern the establishment and maintenance of stable animal-microbe partnerships. This review focuses on what biologists have learned about the developmental trajectory of horizontally acquired symbioses through the study of the binary squid-vibrio model.

We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalo...

Summary: Most 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 squid E uprymna scolopes participates in both: ( i ) selection of the specific partner V ibrio fischeri from the bacterioplankton during symbiosis onset and, ( ii ) modulation of V . fischeri growth 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, esgal1 expression 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 which V . fischeri cells aggregate before migration into the organ. Growth assays revealed that one repeat of EsGal1 arrested growth of G ram‐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 of V . fischeri in 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.

Advances in molecular biology over the last decade have enabled researchers to identify and characterize microbial partners that live in association with animals. These data have indicated that symbiosis is the rule rather than the exception among animals and that interactions with microbes are essential for animal health. This chapter focuses on what we have learned about how such associations influence animal developmental programs. The chapter first considers the‘fingerprin’ of evolutionary circumstances on development of particular animal features. Specifically, the selective forces that have shaped the development of form and function of the immune and digestive systems over evolutionary history are likely to have been strongly influenced by the radiation of animal phyla in the microbe-rich marine environment. The subsequent sections of the chapter consider what biologists have learned and are learning about how microbes influence each stage of development, from the egg through maturation to the adult animal. Particular emphasis is placed on recent findings on the impact of symbiosis on gut development, immunology, brain development, and normal behaviour of the animal host.

Recent molecular data place microbes at the center of the biosphere, from ecosystem sustainability to animal and plant fitness. Models, including the squid-vibrio symbiosis described in this Essay, provide windows into underlying mechanisms that drive these systems.

The symbiotic association between the Hawaiian bobtail squid Euprymna scolopes and the luminous marine bacterium Vibrio fischeri provides a unique opportunity to study epithelial morphogenesis. Sho...