Dataset Information

The Vibrio-Squid Symbiosis as a Model for Studying Interbacterial Competition.

ABSTRACT: The symbiosis between Euprymna scolopes squid and its bioluminescent bacterial symbiont, Vibrio fischeri, is a valuable model system to study a natural, coevolved host-microbe association. Over the past 30 years, researchers have developed and optimized many experimental methods to study both partners in isolation and during symbiosis. These powerful tools, along with a strong foundational knowledge about the system, position the Vibrio-squid symbiosis at the forefront of host-microbe interactions because this system is uniquely suited to investigation of symbiosis from both host and bacterial perspectives. Moreover, the ability to isolate and characterize different strains of V. fischeri has revealed exciting new insights about how different genotypes evolve to compete for a host niche, including deploying interbacterial weapons early during host colonization. This Perspective explores how interbacterial warfare influences the diversity and spatial structure of the symbiotic population, as well as the possible effects that intraspecific competition might have on the host.

SUBMITTER: Septer AN

PROVIDER: S-EPMC6584871 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

The Vibrio-Squid Symbiosis as a Model for Studying Interbacterial Competition.

Septer Alecia N AN

mSystems 20190611 3

The symbiosis between Euprymna scolopes squid and its bioluminescent bacterial symbiont, Vibrio fischeri, is a valuable model system to study a natural, coevolved host-microbe association. Over the past 30 years, researchers have developed and optimized many experimental methods to study both partners in isolation and during symbiosis. These powerful tools, along with a strong foundational knowledge about the system, position the Vibrio-squid symbiosis at the forefront of ho ...[more]

PMID: 31186308

Similar Datasets

Project description:The squid Euprymna scolopes and the luminescent bacterium Vibrio fischeri form a highly specific beneficial light organ symbiosis. Not only does the host have to select V. fischeri from the environment, but it must also prevent subsequent colonization by non-symbiotic microorganisms. Host macrophage-like hemocytes are believed to play a role in mediating the symbiosis with V. fischeri. Previous studies have shown that the colonization state of the light organ influences the host's hemocyte response to the symbiont. To further understand the molecular mechanisms behind this process, we used two quantitative mass-spectrometry-based proteomic techniques, isobaric tags for relative and absolute quantification (iTRAQ) and label-free spectral counting, to compare and quantify the adult hemocyte proteomes from colonized (sym) and uncolonized (antibiotic-treated/cured) squid. Overall, iTRAQ allowed for the quantification of 1,024 proteins with two or more peptides. Thirty-seven unique proteins were determined to be significantly different between sym and cured hemocytes (p value < 0.05), with 20 more abundant proteins and 17 less abundant in sym hemocytes. The label-free approach resulted in 1,241 proteins that were identified in all replicates. Of 185 unique proteins present at significantly different amounts in sym hemocytes (as determined by spectral counting), 92 were more abundant and 93 were less abundant. Comparisons between iTRAQ and spectral counting revealed that 30 of the 37 proteins quantified via iTRAQ exhibited trends similar to those identified by the label-free method. Both proteomic techniques mutually identified 16 proteins that were significantly different between the two groups of hemocytes (p value < 0.05). The presence of V. fischeri in the host light organ influenced the abundance of proteins associated with the cytoskeleton, adhesion, lysosomes, proteolysis, and the innate immune response. These data provide evidence that colonization by V. fischeri alters the hemocyte proteome and reveals proteins that may be important for maintaining host-symbiont specificity.

Project description:UnlabelledThe synergistic activity of Vibrio fischeri lipid A and the peptidoglycan monomer (tracheal cytotoxin [TCT]) induces apoptosis in the superficial cells of the juvenile Euprymna scolopes light organ during the onset of the squid-vibrio symbiosis. Once the association is established in the epithelium-lined crypts of the light organ, the host degrades the symbiont's constitutively produced TCT by the amidase activity of a peptidoglycan recognition protein (E. scolopes peptidoglycan recognition protein 2 [EsPGRP2]). In the present study, we explored the role of alkaline phosphatases in transforming the lipid A of the symbiont into a form that changes its signaling properties to host tissues. We obtained full-length open reading frames for two E. scolopes alkaline phosphatase (EsAP) mRNAs (esap1 and esap2); transcript levels suggested that the dominant light organ isoform is EsAP1. Levels of total EsAP activity increased with symbiosis, but only after the lipid A-dependent morphogenetic induction at 12 h, and were regulated over the day-night cycle. Inhibition of total EsAP activity impaired normal colonization and persistence by the symbiont. EsAP activity localized to the internal regions of the symbiotic juvenile light organ, including the lumina of the crypt spaces where the symbiont resides. These data provide evidence that EsAPs work in concert with EsPGRPs to change the signaling properties of bacterial products and thereby promote persistent colonization by the mutualistic symbiont.ImportanceThe potential for microbe-associated molecular patterns (MAMPs) to compromise host-tissue health is reflected in the often-used nomenclature for these molecules: lipopolysaccharide (LPS) is also called "endotoxin" and the peptidoglycan monomer is also called "tracheal cytotoxin" (TCT). With constant presentation of MAMPs by the normal microbiota, mechanisms to tolerate their effects have developed. The results of this contribution provide evidence that host alkaline phosphatases (APs) dephosphorylate and inactivate the symbiont MAMP lipid A. As such, APs work in synergy with a peptidoglycan recognition protein, which inactivates symbiont-exported TCT, to alter the symbiont MAMPs and promote persistence of the partnership. Not only may these activities serve to "tame" the MAMPs, but also the resulting products may themselves be important signals in persistent mutualisms. The finding of lipid A modification by APs in an invertebrate mutualism provides evidence that this specific strategy for dealing with symbiotic partners is conserved across the animal kingdom.

Dataset Information

The Vibrio-Squid Symbiosis as a Model for Studying Interbacterial Competition.

Publications

The <i>Vibrio</i>-Squid Symbiosis as a Model for Studying Interbacterial Competition.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets