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

mSystems ◽  
2019 ◽  
Vol 4 (3) ◽  
Author(s):  
Alecia N. Septer
Keyword(s):  
Vibrio Fischeri ◽  
Experimental Methods ◽  
Model System ◽  
Bacterial Symbiont ◽  
Euprymna Scolopes ◽  
Content Type ◽  
The Past ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Different Strains

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.

scholarly journals Adaptation to pH stress by Vibrio fischeri can affect its symbiosis with the Hawaiian bobtail squid (Euprymna scolopes)

Microbiology ◽  
2020 ◽  
Vol 166 (3) ◽  
pp. 262-277 ◽  
Author(s):  
Meagan Leah Cohen ◽  
Ekaterina Vadimovna Mashanova ◽  
Sveta Vivian Jagannathan ◽  
William Soto
Keyword(s):  
Type Species ◽  
Vibrio Fischeri ◽  
Acid Stress ◽  
Alkaline Stress ◽  
Euprymna Scolopes ◽  
Free Living ◽  
Content Type ◽  
Link Type ◽  
Microbe Interactions ◽  
Host Microbe Interactions

Many microorganisms engaged in host-microbe interactions pendulate between a free-living phase and a host-affiliated stage. How adaptation to stress during the free-living phase affects host-microbe associations is unclear and understudied. To explore this topic, the symbiosis between Hawaiian bobtail squid (Euprymna scolopes) and the luminous bacterium Vibrio fischeri was leveraged for a microbial experimental evolution study. V. fischeri experienced adaptation to extreme pH while apart from the squid host. V. fischeri was serially passaged for 2000 generations to the lower and upper pH growth limits for this microorganism, which were pH 6.0 and 10.0, respectively. V. fischeri was also serially passaged for 2000 generations to vacillating pH 6.0 and 10.0. Evolution to pH stress both facilitated and impaired symbiosis. Microbial evolution to acid stress promoted squid colonization and increased bioluminescence for V. fischeri , while symbiont adaptation to alkaline stress diminished these two traits. Oscillatory selection to acid and alkaline stress also improved symbiosis for V. fischeri , but the facilitating effects were less than that provided by microbial adaptation to acid stress. In summary, microbial adaptation to harsh environments amid the free-living phase may impact the evolution of host-microbe interactions in ways that were not formerly considered.

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 Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

2016 ◽  
Vol 82 (19) ◽  
pp. 5990-5996 ◽  
Author(s):  
Subhash C. Verma ◽  
Tim Miyashiro
Keyword(s):  
Vibrio Fischeri ◽  
Fundamental Aspect ◽  
Light Organ ◽  
Content Type ◽  
Host Environment ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Microbial Symbionts ◽  
Function Relationship ◽  
The Impact

ABSTRACTHow the function of microbial symbionts is affected by their population/consortium structure within a host remains poorly understood. The symbiosis established betweenEuprymna scolopesandVibrio fischeriis a well-characterized host-microbe association in which the function and structure ofV. fischeripopulations within the host are known:V. fischeripopulations produce bioluminescence from distinct crypt spaces within a dedicated host structure called the light organ. Previous studies have revealed that luminescence is required forV. fischeripopulations to persist within the light organ and that deletion of theluxgene locus, which is responsible for luminescence inV. fischeri, leads to a persistence defect. In this study, we investigated the impact of bioluminescence onV. fischeripopulation structure within the light organ. We report that the persistence defect is specific to crypt I, which is the most developmentally mature crypt space within the nascent light organ. This result provides insight into the structure/function relationship that will be useful for future mechanistic studies of squid-Vibriosymbiosis. In addition, our report highlights the potential impact of the host developmental program on the spatiotemporal dynamics of host-microbe interactions.IMPORTANCEMetazoan development and physiology depend on microbes. The relationship between the symbiotic function of microbes and their spatial structure within the host environment remains poorly understood. Here we demonstrate, using a binary symbiosis, that the host requirement for the symbiotic function of the microbial symbiont is restricted to a specific host environment. Our results also suggest a link between microbial function and host development that may be a fundamental aspect of the more complex host-microbe interactions.

scholarly journals Bactericidal Permeability-Increasing Proteins Shape Host-Microbe Interactions

mBio ◽  
2017 ◽  
Vol 8 (2) ◽  
Author(s):  
Fangmin Chen ◽  
Benjamin C. Krasity ◽  
Suzanne M. Peyer ◽  
Sabrina Koehler ◽  
Edward G. Ruby ◽  
...  
Keyword(s):  
Antimicrobial Activity ◽  
Vibrio Fischeri ◽  
Molecular Characteristics ◽  
Light Organ ◽  
Euprymna Scolopes ◽  
Lipopolysaccharide Binding Protein ◽  
Ambient Seawater ◽  
Microbe Interactions ◽  
Acidic Conditions ◽  
Host Microbe Interactions

ABSTRACT We characterized bactericidal permeability-increasing proteins (BPIs) of the squid Euprymna scolopes , EsBPI2 and EsBPI4. They have molecular characteristics typical of other animal BPIs, are closely related to one another, and nest phylogenetically among invertebrate BPIs. Purified EsBPIs had antimicrobial activity against the squid’s symbiont, Vibrio fischeri , which colonizes light organ crypt epithelia. Activity of both proteins was abrogated by heat treatment and coincubation with specific antibodies. Pretreatment under acidic conditions similar to those during symbiosis initiation rendered V. fischeri more resistant to the antimicrobial activity of the proteins. Immunocytochemistry localized EsBPIs to the symbiotic organ and other epithelial surfaces interacting with ambient seawater. The proteins differed in intracellular distribution. Further, whereas EsBPI4 was restricted to epithelia, EsBPI2 also occurred in blood and in a transient juvenile organ that mediates hatching. The data provide evidence that these BPIs play different defensive roles early in the life of E. scolopes , modulating interactions with the symbiont. IMPORTANCE This study describes new functions for bactericidal permeability-increasing proteins (BPIs), members of the lipopolysaccharide-binding protein (LBP)/BPI protein family. The data provide evidence that these proteins play a dual role in the modulation of symbiotic bacteria. In the squid-vibrio model, these proteins both control the symbiont populations in the light organ tissues where symbiont cells occur in dense monoculture and, concomitantly, inhibit the symbiont from colonizing other epithelial surfaces of the animal.

scholarly journals Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis

mBio ◽  
2019 ◽  
Vol 10 (6) ◽  
Author(s):  
Tjorven Hinzke ◽  
Manuel Kleiner ◽  
Corinna Breusing ◽  
Horst Felbeck ◽  
Robert Häsler ◽  
...  
Keyword(s):  
Deep Sea ◽  
Population Control ◽  
Sequence Information ◽  
Riftia Pachyptila ◽  
Content Type ◽  
Intracellular Symbiont ◽  
Energy Limitation ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Substrate Transfer

ABSTRACT The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis. IMPORTANCE All animals are associated with microorganisms; hence, host-microbe interactions are of fundamental importance for life on earth. However, we know little about the molecular basis of these interactions. Therefore, we studied the deep-sea Riftia pachyptila symbiosis, a model association in which the tubeworm host is associated with only one phylotype of endosymbiotic bacteria and completely depends on this sulfur-oxidizing symbiont for nutrition. Using a metaproteomics approach, we identified both metabolic interaction processes, such as substrate transfer between the two partners, and interactions that serve to maintain the symbiotic balance, e.g., host efforts to control the symbiont population or symbiont strategies to modulate these host efforts. We suggest that these interactions are essential principles of mutualistic animal-microbe associations.

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 Human Three-Dimensional Endometrial Epithelial Cell Model To Study Host Interactions with Vaginal Bacteria and Neisseria gonorrhoeae

2017 ◽  
Vol 85 (3) ◽  
Author(s):  
Paweł Łaniewski ◽  
Adriana Gomez ◽  
Geoffrey Hire ◽  
Magdalene So ◽  
Melissa M. Herbst-Kralovetz
Keyword(s):  
Epithelial Cell ◽  
Neisseria Gonorrhoeae ◽  
Pathogenic Bacteria ◽  
Three Dimensional ◽  
Female Reproductive Tract ◽  
Content Type ◽  
Endometrial Epithelial Cell ◽  
Proinflammatory Mediators ◽  
Microbe Interactions ◽  
Host Microbe Interactions

ABSTRACT Colonization of the endometrium by pathogenic bacteria ascending from the lower female reproductive tract (FRT) is associated with many gynecologic and obstetric health complications. To study these host-microbe interactions in vitro, we developed a human three-dimensional (3-D) endometrial epithelial cell (EEC) model using the HEC-1A cell line and the rotating wall vessel (RWV) bioreactor technology. Our model, composed of 3-D EEC aggregates, recapitulates several functional/structural characteristics of human endometrial epithelial tissue, including cell differentiation, the presence of junctional complexes/desmosomes and microvilli, and the production of membrane-associated mucins and Toll-like receptors (TLRs). TLR function was evaluated by exposing the EEC aggregates to viral and bacterial products. Treatment with poly(I·C) and flagellin but not with synthetic lipoprotein (fibroblast-stimulating lipoprotein 1 [FSL-1]) or lipopolysaccharide (LPS) significantly induced proinflammatory mediators in a dose-dependent manner. To simulate ascending infection, we infected EEC aggregates with commensal and pathogenic bacteria: Lactobacillus crispatus, Gardnerella vaginalis, and Neisseria gonorrhoeae. All vaginal microbiota and N. gonorrhoeae efficiently colonized the 3-D surface, localizing to crevices of the EEC model and interacting with multiple adjacent cells simultaneously. However, only infection with pathogenic N. gonorrhoeae and not infection with the other bacteria tested significantly induced proinflammatory mediators and significant ultrastructural changes to the host cells. The latter observation is consistent with clinical findings and illustrated the functional specificity of our system. Additionally, we highlighted the utility of the 3-D EEC model for the study of the pathogenesis of N. gonorrhoeae using a well-characterized ΔpilT mutant. Overall, this study demonstrates that the human 3-D EEC model is a robust tool for studying host-microbe interactions and bacterial pathogenesis in the upper FRT.

scholarly journals Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts

mBio ◽  
2015 ◽  
Vol 6 (3) ◽  
Author(s):  
Kristen E. Murfin ◽  
Ming-Min Lee ◽  
Jonathan L. Klassen ◽  
Bradon R. McDonald ◽  
Bret Larget ◽  
...  
Keyword(s):  
Bacterial Strain ◽  
Bacterial Symbiont ◽  
Evolutionary Time ◽  
Strain Diversity ◽  
Microbe Interactions ◽  
Fitness Benefits ◽  
Host Microbe Interactions ◽  
Microbial Symbionts ◽  
Term Maintenance

ABSTRACTMicrobial symbionts provide benefits that contribute to the ecology and fitness of host plants and animals. Therefore, the evolutionary success of plants and animals fundamentally depends on long-term maintenance of beneficial associations. Most work investigating coevolution and symbiotic maintenance has focused on species-level associations, and studies are lacking that assess the impact of bacterial strain diversity on symbiotic associations within a coevolutionary framework. Here, we demonstrate that fitness in mutualism varies depending on bacterial strain identity, and this is consistent with variation shaping phylogenetic patterns and maintenance through fitness benefits. Through genome sequencing of nine bacterial symbiont strains and cophylogenetic analysis, we demonstrate diversity amongXenorhabdus bovieniibacteria. Further, we identified cocladogenesis betweenSteinernema feltiaenematode hosts and their correspondingX. bovieniisymbiont strains, indicating potential specificity within the association. To test the specificity, we performed laboratory crosses of nematode hosts with native and nonnative symbiont strains, which revealed that combinations with the native bacterial symbiont and closely related strains performed significantly better than those with more divergent symbionts. Through genomic analyses we also defined potential factors contributing to specificity between nematode hosts and bacterial symbionts. These results suggest that strain-level diversity (e.g., subspecies-level differences) in microbial symbionts can drive variation in the success of host-microbe associations, and this suggests that these differences in symbiotic success could contribute to maintenance of the symbiosis over an evolutionary time scale.IMPORTANCEBeneficial symbioses between microbes and plant or animal hosts are ubiquitous, and in these associations, microbial symbionts provide key benefits to their hosts. As such, host success is fundamentally dependent on long-term maintenance of beneficial associations. Prolonged association between partners in evolutionary time is expected to result in interactions in which only specific partners can fully support symbiosis. The contribution of bacterial strain diversity on specificity and coevolution in a beneficial symbiosis remains unclear. In this study, we demonstrate that strain-level differences in fitness benefits occur in beneficial host-microbe interactions, and this variation likely shapes phylogenetic patterns and symbiotic maintenance. This highlights that symbiont contributions to host biology can vary significantly based on very-fine-scale differences among members of a microbial species. Further, this work emphasizes the need for greater phylogenetic resolution when considering the causes and consequences of host-microbe interactions.

scholarly journals Modulation of the Host Cell Transcriptome and Epigenome by Fusobacterium nucleatum

mBio ◽  
2021 ◽  
Vol 12 (5) ◽  
Author(s):  
Cody A. Despins ◽  
Scott D. Brown ◽  
Avery V. Robinson ◽  
Andrew J. Mungall ◽  
Emma Allen-Vercoe ◽  
...  
Keyword(s):  
Colorectal Cancer ◽  
Oral Cavity ◽  
Host Cell ◽  
Treatment Resistance ◽  
Fusobacterium Nucleatum ◽  
Content Type ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Cell Transcriptome ◽  
Cancer Settings

Fusobacterium nucleatum is a bacterium normally found in the healthy oral cavity but also has an emerging role in colorectal cancer and other cancer settings. The host-microbe interactions of F. nucleatum and its involvement in tumor initiation, progression, and treatment resistance are not fully understood.

Sign in / Sign up

Export Citation Format

Share Document