Getting the Message Out: the Many Modes of Host-Symbiont Communication during Early-Stage Establishment of the Squid-Vibrio Partnership

McFall‐Ngai, Margaret J.; Ruby, Edward G.

doi:10.1128/msystems.00867-21

Cited by 4 publications

(3 citation statements)

References 54 publications

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“…The host detects these PG fragments as a sign that bacteria are present. However, in some commensal or mutualistic Gram-negative species, significant amounts of the PG monomer are released, which acts as a signal mediating a specific response in the epithelium of susceptible hosts ( 47 , 56 ).…”

Section: Discussionmentioning

confidence: 99%

Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

Montoya-Ciriaco,

Hereira-Pacheco,

Estrada-Torres

et al. 2023

Microbiol Spectr

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The maternal transmission of microbiota during embryonic development of vertebrates is still poorly understood. Here, we used high-throughput sequencing of the 16S rRNA bacterial genes to determine the bacterial communities in the gastrointestinal tract and amniotic environment, i.e., the amniotic fluid, amniotic membrane and extraembryonic yolk, of embryos at the last stage of development of the viviparous lizard Sceloporus grammicus Wiegmann, 1828. We compared these communities to those found in the maternal intestine, mouth, cloaca, and the aseptic ventral skin as a control of the aseptic technique. Our results showed that bacterial 16S rRNA genes were present in the embryos of S. grammicus . Their diversity was lower and more similar in composition between individuals than those found in the maternal tissues. This suggests that a strong control exists on the transmission of bacteria from the mother to the embryos. We found 78% of the embryonic amplicon sequence variants (ASVs) in the maternal bacterial microbiota, suggesting that the transmission of bacteria from the mother to the embryos is a continuous process and some bacteria may have been transferred during early embryonic stages. The embryonic bacteria were found to overlap mostly with those found in the mouth and aseptic ventral skin of the mother, although it is difficult to conclude that the shared ASVs originated from these maternal tissues. Our study provides evidence of microbiota vertical transfer during embryonic development in the animal kingdom. It also highlights that this maternal transmission could be included in the maternal effects that impact the offspring. IMPORTANCE We investigated the presence and diversity of bacteria in the embryos of the viviparous lizard Sceloporus grammicus and their amniotic environment. We compared this diversity to that found in the maternal intestine, mouth, and cloaca. We detected bacterial DNA in the embryos, albeit with a lower bacterial species diversity than found in maternal tissues. Most of the bacterial species detected in the embryos were also found in the mother, although not all of them. Interestingly, we detected a high similarity in the composition of bacterial species among embryos from different mothers. These findings suggest that there may be a mechanism controlling the transmission of bacteria from the mother to the embryo. Our results highlight the possibility that the interaction between maternal bacteria and the embryo may affect the development of the lizards.

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Section: Discussionmentioning

confidence: 99%

Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

Montoya-Ciriaco,

Hereira-Pacheco,

Estrada-Torres

et al. 2023

Microbiol Spectr

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“…The sepiolid squid– Vibrio partnership is a powerful invertebrate–bacterial model system for better understanding inter-organismal communication in beneficial associations [ 102 ]. It is a simple binary open symbiosis where both the host and symbiont can be grown and manipulated separately before introducing them together.…”

Section: Discussionmentioning

confidence: 99%

Nocturnal Acidification: A Coordinating Cue in the Euprymna scolopes–Vibrio fischeri Symbiosis

Pipes

Nishiguchi

2022

IJMS

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The Vibrio fischeri–Euprymna scolopes symbiosis has become a powerful model for the study of specificity, initiation, and maintenance between beneficial bacteria and their eukaryotic partner. In this invertebrate model system, the bacterial symbionts are acquired every generation from the surrounding seawater by newly hatched squid. These symbionts colonize a specialized internal structure called the light organ, which they inhabit for the remainder of the host’s lifetime. The V. fischeri population grows and ebbs following a diel cycle, with high cell densities at night producing bioluminescence that helps the host avoid predation during its nocturnal activities. Rhythmic timing of the growth of the symbionts and their production of bioluminescence only at night is critical for maintaining the symbiosis. V. fischeri symbionts detect their population densities through a behavior termed quorum-sensing, where they secrete and detect concentrations of autoinducer molecules at high cell density when nocturnal production of bioluminescence begins. In this review, we discuss events that lead up to the nocturnal acidification of the light organ and the cues used for pre-adaptive behaviors that both host and symbiont have evolved. This host–bacterium cross talk is used to coordinate networks of regulatory signals (such as quorum-sensing and bioluminescence) that eventually provide a unique yet stable environment for V. fischeri to thrive and be maintained throughout its life history as a successful partner in this dynamic symbiosis.

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“…In the squid-vibrio symbiosis, the horizontally transmitted bacterium V. fischeri receives host nutrients in exchange for providing bioluminescence that is used as counterillumination by the squid for nocturnal camouflage (Ruby & McFall-Ngai, 1992). The symbiosis is induced by a molecular dialogue between host and symbiont, where V. fischeri colonises and establishes itself within a specialised bilobed light organ within the squid with each lobe containing three epithelial lined crypt spaces where the bacteria reside and grow (Figure 1A-E; McFall-Ngai & Ruby, 2021). The bacteria are harvested from the environment by ciliated epithelial appendages located on the surface of the light organ, which bring V. fischeri near pores that lead into the light organ (Figure 1B; Nawroth et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Modelled microgravity impacts Vibrio fischeri population structure in a mutualistic association with an animal host

Bongrand,

Foster

2023

Environmental Microbiology

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Perturbations to host–microbe interactions, such as environmental stress, can alter and disrupt homeostasis. In this study, we examined the effects of a stressor, simulated microgravity, on beneficial bacteria behaviours when colonising their host. We studied the bacterium Vibrio fischeri, which establishes a mutualistic association in a symbiosis‐specific organ within the bobtail squid, Euprymna scolopes. To elucidate how animal–microbe interactions are affected by the stress of microgravity, squid were inoculated with different bacterial strains exhibiting either a dominant‐ or sharing‐colonisation behaviour in High Aspect Ratio Vessels, which simulate the low‐shear environment of microgravity. The colonisation behaviours of the sharing and dominant strains under modelled microgravity conditions were determined by counting light‐organ homogenate of squids as well as confocal microscopy to assess the partitioning of different strains within the light organ. The results indicated that although the colonisation behaviours of the strains did not change, the population levels of the sharing strains were at lower relative abundance in single‐colonised animals exposed to modelled microgravity compared to unit gravity; in addition, there were shifts in the relative abundance of strains in co‐colonised squids. Together these results suggest that the initiation of beneficial interactions between microbes and animals can be altered by environmental stress, such as simulated microgravity.

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Getting the Message Out: the Many Modes of Host-Symbiont Communication during Early-Stage Establishment of the Squid-Vibrio Partnership

Cited by 4 publications

References 54 publications

Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

Nocturnal Acidification: A Coordinating Cue in the Euprymna scolopes–Vibrio fischeri Symbiosis

Modelled microgravity impacts Vibrio fischeri population structure in a mutualistic association with an animal host

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