The Importance of Microbes in Animal Development: Lessons from the Squid-Vibrio Symbiosis

Abstract

Developmental biology is among the many sub-disciplines 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., 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 into the environment. 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 upon what biologists have learned about the developmental trajectory of horizontally acquired symbioses through the study of the binary squid-vibrio model.

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

“…To address whether OMVs produced by V. fischeri present morphogenesis-inducing MAMPs to the host, we first asked whether the OMVs trigger two morphogenic changes known to be induced by the synergy of PG fragments and LPS: late apoptosis in and regression of the light organ's surface epithelial fields (6). We found that on its own, OMV addition induces pronounced levels of late-stage apoptosis after 24 h (Fig.…”

“…OMV production is increased in a Helicobacter tolB mutant with an altered interaction with OMPs (31), indicating a connection between these membranestabilizing proteins and the rate of OMV generation (32,33). Similarly, OmpU, the major OMP of Vibrio spp., plays roles in both pathogenesis and symbiosis within this genus (6,34). For instance, in pathogenic relationships, OmpU facilitates colonization (35), allowing binding to host tissue and inducing specific immune responses, including cell death (36)(37)(38).…”

“…OMVs were separated from other extracellular products by ultracentrifugation at 173,000 ϫ g for 2 h at 4°C in a 90 Ti rotor (Beckman Coulter, Inc., Brea, CA). The resulting pellet was washed and resuspended in Dulbecco's phosphate-buffered saline (dPBS) (0.2 g of KCl, 0.2 g of KH 2 PO 4 , 11.7 g of NaCl, 1.1 g of Na 2 HPO 4 , 0.1 g of MgCl 2 (H 2 O) 6 , and 0.1 g of CaCl 2 per liter of deionized water), supplemented with an additional 11.7 g/liter NaCl, and filter sterilized. The protein concentration of OMVs was determined using a Qubit 2.0 fluorometer (Life Technologies, Grand Island, NY), according to the manu- Quantification of OMVs by total-lipid and LPS assays.…”

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

“…Natural invertebrate model systems that maintain one or a few symbiotic microbial species, such as nematodes, medicinal leeches, and squid (15), provide a window through which we can discover themes conserved across the diversity of interactions of animals with their coevolved microbiota, whether simple or complex. In particular, the symbiosis of the bobtail squid Euprymna scolopes and the luminous bacterium Vibrio fischeri, in which the microbial symbiont can be manipulated without compromising the health of the host, presents a rare opportunity to study the chemical and immune dialogues of symbiotic partners at a cellular and molecular level (16).…”

Bacterial type VI secretion system facilitates niche domination

“…Speare et al (6) investigate the early stages of squid colonization, when the hatchling acquires its symbiotic partner from the surrounding seawater. While several mechanisms have been elucidated that contribute to the unique selection of V. fischeri as the sole symbiont of the animal's light organ (14), the underlying molecular mechanism of a recent discovery, namely that crypts are rarely cocolonized by more than one strain of V. fischeri (15), remained elusive. This finding suggests that either a bottleneck restricts access to more than a single bacterium, or, as shown here, that interbacterial competition occurs inside the light organ (6).…”