scholarly journals Bacterial Quorum-Sensing Regulation Induces Morphological Change in a Key Host Tissue during the Euprymna scolopes-Vibrio fischeri Symbiosis

mBio ◽  
2021 ◽  
Author(s):  
T. Essock-Burns ◽  
B. D. Bennett ◽  
D. Arencibia ◽  
S. Moriano-Gutierrez ◽  
M. Medeiros ◽  
...  
Keyword(s):  
Quorum Sensing ◽  
Morphological Change ◽  
Vibrio Fischeri ◽  
Host Tissue ◽  
Light Organ ◽  
Euprymna Scolopes ◽  
Content Type ◽  
Bacterial Quorum Sensing ◽  
Colonization Factors ◽  
Bacterial Quorum

Interbacterial signaling within a host-associated population can have profound effects on the behavior of the bacteria, for instance, in their production of virulence/colonization factors; in addition, such signaling can dictate the nature of the outcome for the host, in both pathogenic and beneficial associations. Using the monospecific squid-vibrio model of symbiosis, we examined how quorum-sensing regulation by the Vibrio fischeri population induces a biogeographic tissue phenotype that promotes the retention of this extracellular symbiont within the light organ of its host, Euprymna scolopes .

scholarly journals An Expanded Transposon Mutant Library Reveals that Vibrio fischeri δ-Aminolevulinate Auxotrophs Can Colonize Euprymna scolopes

2016 ◽  
Vol 83 (5) ◽  
Author(s):  
Noreen L. Lyell ◽  
Alecia N. Septer ◽  
Anne K. Dunn ◽  
Drew Duckett ◽  
Julie L. Stoudenmire ◽  
...  
Keyword(s):  
Vibrio Fischeri ◽  
Light Organ ◽  
Mutant Library ◽  
Euprymna Scolopes ◽  
Simple Method ◽  
Content Type ◽  
Transposon Insertion ◽  
Rich Media ◽  
Show Evidence

ABSTRACT Libraries of defined mutants are valuable research tools but necessarily lack gene knockouts that are lethal under the conditions used in library construction. In this study, we augmented a Vibrio fischeri mutant library generated on a rich medium (LBS, which contains [per liter] 10 g of tryptone, 5 g of yeast extract, 20 g of NaCl, and 50 mM Tris [pH 7.5]) by selecting transposon insertion mutants on supplemented LBS and screening for those unable to grow on LBS. We isolated strains with insertions in alr, glr (murI), glmS, several heme biosynthesis genes, and ftsA, as well as a mutant disrupted 14 bp upstream of ftsQ. Mutants with insertions in ftsA or upstream of ftsQ were recovered by addition of Mg2+ to LBS, but their cell morphology and motility were affected. The ftsA mutant was more strongly affected and formed cells or chains of cells that appeared to wind back on themselves helically. Growth of mutants with insertions in glmS, alr, or glr was recovered with N-acetylglucosamine (NAG), d-alanine, or d-glutamate, respectively. We hypothesized that NAG, d-alanine, or d-glutamate might be available to V. fischeri in the Euprymna scolopes light organ; however, none of these mutants colonized the host effectively. In contrast, hemA and hemL mutants, which are auxotrophic for δ-aminolevulinate (ALA), colonized at wild-type levels, although mutants later in the heme biosynthetic pathway were severely impaired or unable to colonize. Our findings parallel observations that legume hosts provide Bradyrhizobium symbionts with ALA, but they contrast with virulence phenotypes of hemA mutants in some pathogens. The results further inform our understanding of the symbiotic light organ environment. IMPORTANCE By supplementing a rich yeast-based medium, we were able to recover V. fischeri mutants with insertions in conditionally essential genes, and further characterization of these mutants provided new insights into this bacterium's symbiotic environment. Most notably, we show evidence that the squid host can provide V. fischeri with enough ALA to support its growth in the light organ, paralleling the finding that legumes provide Bradyrhizobium ALA in symbiotic nodules. Taken together, our results show how a simple method of augmenting already rich media can expand the reach and utility of defined mutant libraries.

scholarly journals Implications of Rewiring Bacterial Quorum Sensing

2007 ◽  
Vol 74 (2) ◽  
pp. 437-445 ◽  
Author(s):  
Eric L. Haseltine ◽  
Frances H. Arnold
Keyword(s):  
Gene Expression ◽  
Quorum Sensing ◽  
Network Architecture ◽  
Vibrio Fischeri ◽  
Cell Communication ◽  
Biologically Relevant ◽  
Synthetic Gene Circuits ◽  
Bacterial Quorum Sensing ◽  
Forward Engineering ◽  
Bacterial Quorum

ABSTRACT Bacteria employ quorum sensing, a form of cell-cell communication, to sense changes in population density and regulate gene expression accordingly. This work investigated the rewiring of one quorum-sensing module, the lux circuit from the marine bacterium Vibrio fischeri. Steady-state experiments demonstrate that rewiring the network architecture of this module can yield graded, threshold, and bistable gene expression as predicted by a mathematical model. The experiments also show that the native lux operon is most consistent with a threshold, as opposed to a bistable, response. Each of the rewired networks yielded functional population sensors at biologically relevant conditions, suggesting that this operon is particularly robust. These findings (i) permit prediction of the behaviors of quorum-sensing operons in bacterial pathogens and (ii) facilitate forward engineering of synthetic gene circuits.

scholarly journals Interfering with Bacterial Quorum Sensing

2016 ◽  
Vol 8 ◽  
pp. PMC.S13209 ◽  
Author(s):  
Kerstin Reuter ◽  
Anke Steinbach ◽  
Volkhard Helms
Keyword(s):  
Quorum Sensing ◽  
Vibrio Fischeri ◽  
Critical Threshold ◽  
Resistant Bacteria ◽  
Bacterial Cells ◽  
Bacterial Survival ◽  
Bacterial Populations ◽  
Bacterial Quorum Sensing ◽  
Bacterial Quorum ◽  
Molecular Components

Quorum sensing (QS) describes the exchange of chemical signals in bacterial populations to adjust the bacterial phenotypes according to the density of bacterial cells. This serves to express phenotypes that are advantageous for the group and ensure bacterial survival. To do so, bacterial cells synthesize autoinducer (AI) molecules, release them to the environment, and take them up. Thereby, the AI concentration reflects the cell density. When the AI concentration exceeds a critical threshold in the cells, the AI may activate the expression of virulence-associated genes or of luminescent proteins. It has been argued that targeting the QS system puts less selective pressure on these pathogens and should avoid the development of resistant bacteria. Therefore, the molecular components of QS systems have been suggested as promising targets for developing new anti-infective compounds. Here, we review the QS systems of selected gram-negative and gram-positive bacteria, namely, Vibrio fischeri, Pseudomonas aeruginosa, and Staphylococcus aureus, and discuss various antivirulence strategies based on blocking different components of the QS machinery.

scholarly journals HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in Vibrio fischeri

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Brittany D. Bennett ◽  
Tara Essock-Burns ◽  
Edward G. Ruby
Keyword(s):  
Vibrio Fischeri ◽  
Light Organ ◽  
Euprymna Scolopes ◽  
Regulatory Pathway ◽  
Content Type ◽  
Exopolysaccharide Production ◽  
Bioluminescent Bacterium ◽  
Expression Of Genes ◽  
Complex Process ◽  
Virulence Regulator

ABSTRACT The bioluminescent bacterium Vibrio fischeri forms a mutually beneficial symbiosis with the Hawaiian bobtail squid, Euprymna scolopes, in which the bacteria, housed inside a specialized light organ, produce light used by the squid in its nocturnal activities. Upon hatching, E. scolopes juveniles acquire V. fischeri from the seawater through a complex process that requires, among other factors, chemotaxis by the bacteria along a gradient of N-acetylated sugars into the crypts of the light organ, the niche in which the bacteria reside. Once inside the light organ, V. fischeri transitions into a symbiotic, sessile state in which the quorum-signaling regulator LitR induces luminescence. In this work we show that expression of litR and luminescence are repressed by a homolog of the Vibrio cholerae virulence factor TcpP, which we have named HbtR. Further, we demonstrate that LitR represses genes involved in motility and chemotaxis into the light organ and activates genes required for exopolysaccharide production. IMPORTANCE TcpP homologs are widespread throughout the Vibrio genus; however, the only protein in this family described thus far is a V. cholerae virulence regulator. Here, we show that HbtR, the TcpP homolog in V. fischeri, has both a biological role and regulatory pathway completely unlike those in V. cholerae. Through its repression of the quorum-signaling regulator LitR, HbtR affects the expression of genes important for colonization of the E. scolopes light organ. While LitR becomes activated within the crypts and upregulates luminescence and exopolysaccharide genes and downregulates chemotaxis and motility genes, it appears that HbtR, upon expulsion of V. fischeri cells into seawater, reverses this process to aid the switch from a symbiotic to a planktonic state. The possible importance of HbtR to the survival of V. fischeri outside its animal host may have broader implications for the ways in which bacteria transition between often vastly different environmental niches.

scholarly journals Screening of Bacterial Quorum Sensing Inhibitors in a Vibrio fischeri LuxR-Based Synthetic Fluorescent E. coli Biosensor

2020 ◽  
Vol 13 (9) ◽  
pp. 263
Author(s):  
Xiaofei Qin ◽  
Celina Vila-Sanjurjo ◽  
Ratna Singh ◽  
Bodo Philipp ◽  
Francisco M. Goycoolea
Keyword(s):  
Quorum Sensing ◽  
Bacterial Growth ◽  
Vibrio Fischeri ◽  
Caffeic Acid Phenethyl Ester ◽  
Docking Studies ◽  
Inhibition Activity ◽  
E Coli ◽  
Bacterial Quorum Sensing ◽  
Pure Compounds ◽  
Bacterial Quorum

A library of 23 pure compounds of varying structural and chemical characteristics was screened for their quorum sensing (QS) inhibition activity using a synthetic fluorescent Escherichia coli biosensor that incorporates a modified version of lux regulon of Vibrio fischeri. Four such compounds exhibited QS inhibition activity without compromising bacterial growth, namely, phenazine carboxylic acid (PCA), 2-heptyl-3-hydroxy-4-quinolone (PQS), 1H-2-methyl-4-quinolone (MOQ) and genipin. When applied at 50 µM, these compounds reduced the QS response of the biosensor to 33.7% ± 2.6%, 43.1% ± 2.7%, 62.2% ± 6.3% and 43.3% ± 1.2%, respectively. A series of compounds only showed activity when tested at higher concentrations. This was the case of caffeine, which, when applied at 1 mM, reduced the QS to 47% ± 4.2%. In turn, capsaicin, caffeic acid phenethyl ester (CAPE), furanone and polygodial exhibited antibacterial activity when applied at 1mM, and reduced the bacterial growth by 12.8% ± 10.1%, 24.4% ± 7.0%, 91.4% ± 7.4% and 97.5% ± 3.8%, respectively. Similarly, we confirmed that trans-cinnamaldehyde and vanillin, when tested at 1 mM, reduced the QS response to 68.3% ± 4.9% and 27.1% ± 7.4%, respectively, though at the expense of concomitantly reducing cell growth by 18.6% ± 2.5% and 16% ± 2.2%, respectively. Two QS natural compounds of Pseudomonas aeruginosa, namely PQS and PCA, and the related, synthetic compounds MOQ, 1H-3-hydroxyl-4-quinolone (HOQ) and 1H-2-methyl-3-hydroxyl-4-quinolone (MHOQ) were used in molecular docking studies with the binding domain of the QS receptor TraR as a target. We offer here a general interpretation of structure-function relationships in this class of compounds that underpins their potential application as alternatives to antibiotics in controlling bacterial virulence.

scholarly journals A Small Molecule Coordinates Symbiotic Behaviors in a Host Organ

mBio ◽  
2021 ◽  
Vol 12 (2) ◽  
Author(s):  
Katherine E. Zink ◽  
Denise A. Ludvik ◽  
Phillip R. Lazzara ◽  
Terry W. Moore ◽  
Mark J. Mandel ◽  
...  
Keyword(s):  
Mass Spectrometry ◽  
Small Molecules ◽  
Vibrio Fischeri ◽  
Imaging Mass Spectrometry ◽  
Light Organ ◽  
Euprymna Scolopes ◽  
Content Type ◽  
Bacterial Luminescence ◽  
Microbe Interactions ◽  
Host Microbe Interactions

ABSTRACT The lifelong relationship between the Hawaiian bobtail squid Euprymna scolopes and its microbial symbiont Vibrio fischeri represents a simplified model system for studying microbiome establishment and maintenance. The bacteria colonize a dedicated symbiotic light organ in the squid, from which bacterial luminescence camouflages the host in a process termed counterillumination. The squid host hatches without its symbionts, which must be acquired from the ocean amidst a diversity of nonbeneficial bacteria, such that precise molecular communication is required for initiation of the specific relationship. Therefore it is likely there are specialized metabolites used in the light organ microenvironment to modulate these processes. To identify small molecules that may influence the establishment of this symbiosis, we used imaging mass spectrometry to analyze metabolite production in V. fischeri with altered biofilm production, which correlates directly to colonization capability in its host. “Biofilm-up” and “biofilm-down” mutants were compared to a wild-type strain, and ions that were more abundantly produced by the biofilm-up mutant were detected. Using a combination of structural elucidation and synthetic chemistry, one such signal was determined to be a diketopiperazine, cyclo(d-histidyl-l-proline). This diketopiperazine modulated luminescence in V. fischeri and, using imaging mass spectrometry, was directly detected in the light organ of the colonized host. This work highlights the continued need for untargeted discovery efforts in host-microbe interactions and showcases the benefits of the squid-Vibrio system for identification and characterization of small molecules that modulate microbiome behaviors. IMPORTANCE The complexity of animal microbiomes presents challenges to defining signaling molecules within the microbial consortium and between the microbes and the host. By focusing on the binary symbiosis between Vibrio fischeri and Euprymna scolopes, we have combined genetic analysis with direct imaging to define and study small molecules in the intact symbiosis. We have detected and characterized a diketopiperazine produced by strong biofilm-forming V. fischeri strains that was detectable in the host symbiotic organ, and which influences bacterial luminescence. Biofilm formation and luminescence are critical for initiation and maintenance of the association, respectively, suggesting that the compound may link early and later development stages, providing further evidence that multiple small molecules are important in establishing these beneficial relationships.

scholarly journals Squid-Derived Chitin Oligosaccharides Are a Chemotactic Signal during Colonization by Vibrio fischeri

2012 ◽  
Vol 78 (13) ◽  
pp. 4620-4626 ◽  
Author(s):  
Mark J. Mandel ◽  
Amy L. Schaefer ◽  
Caitlin A. Brennan ◽  
Elizabeth A. C. Heath-Heckman ◽  
Cindy R. DeLoney-Marino ◽  
...  
Keyword(s):  
Vibrio Fischeri ◽  
Attachment Site ◽  
Light Organ ◽  
Euprymna Scolopes ◽  
Luminous Bacterium ◽  
Content Type ◽  
Light Emitting ◽  
Marine Luminous Bacterium ◽  
The Family ◽  
Host Generation

ABSTRACTChitin, a polymer ofN-acetylglucosamine (GlcNAc), is noted as the second most abundant biopolymer in nature. Chitin serves many functions for marine bacteria in the familyVibrionaceae(“vibrios”), in some instances providing a physical attachment site, inducing natural genetic competence, and serving as an attractant for chemotaxis. The marine luminous bacteriumVibrio fischeriis the specific symbiont in the light-emitting organ of the Hawaiian bobtail squid,Euprymna scolopes. The bacterium provides the squid with luminescence that the animal uses in an antipredatory defense, while the squid supports the symbiont's nutritional requirements.V. fischericells are harvested from seawater during each host generation, andV. fischeriis the only species that can complete this process in nature. Furthermore, chitin is located in squid hemocytes and plays a nutritional role in the symbiosis. We demonstrate here that chitin oligosaccharides produced by the squid host serve as a chemotactic signal for colonizing bacteria.V. fischeriuses the gradient of host chitin to enter the squid light organ duct and colonize the animal. We provide evidence that chitin serves a novel function in an animal-bacterial mutualism, as an animal-produced bacterium-attracting synomone.

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