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 Host-microbe interactions in the chemosyntheticRiftia pachyptilasymbiosis

2019 ◽  
Author(s):  
Tjorven Hinzke ◽  
Manuel Kleiner ◽  
Corinna Breusing ◽  
Horst Felbeck ◽  
Robert Häsler ◽  
...  
Keyword(s):  
Population Control ◽  
Sequence Information ◽  
Riftia Pachyptila ◽  
Host Proteins ◽  
Intracellular Symbiont ◽  
Energy Limitation ◽  
Bacterial Endosymbionts ◽  
Microbe Interactions ◽  
Metabolic Interactions ◽  
Host Microbe Interactions

AbstractThe deep-sea tubewormRiftia pachyptilalacks 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 theRiftiatranscriptome, which enabled comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. We demonstrate that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion, and substrate transfer to the symbiont by abundant host proteins. Our analysis further suggests thatRiftiamaintains 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.

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 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.

scholarly journals Multiple evolutionary origins reflect the importance of sialic acid transporters in the colonization potential of bacterial pathogens and commensals

2021 ◽  
Vol 7 (6) ◽  
Author(s):  
Emmanuele Severi ◽  
Michelle Rudden ◽  
Andrew Bell ◽  
Tracy Palmer ◽  
Nathalie Juge ◽  
...  
Keyword(s):  
Phylogenetic Analysis ◽  
Sialic Acid ◽  
Sialic Acids ◽  
Content Type ◽  
Link Type ◽  
Evolutionary Origins ◽  
Mucosal Surfaces ◽  
Colonization Potential ◽  
Microbe Interactions ◽  
Host Microbe Interactions

Located at the tip of cell surface glycoconjugates, sialic acids are at the forefront of host–microbe interactions and, being easily liberated by sialidase enzymes, are used as metabolites by numerous bacteria, particularly by pathogens and commensals living on or near diverse mucosal surfaces. These bacteria rely on specific transporters for the acquisition of host-derived sialic acids. Here, we present the first comprehensive genomic and phylogenetic analysis of bacterial sialic acid transporters, leading to the identification of multiple new families and subfamilies. Our phylogenetic analysis suggests that sialic acid-specific transport has evolved independently at least eight times during the evolution of bacteria, from within four of the major families/superfamilies of bacterial transporters, and we propose a robust classification scheme to bring together a myriad of different nomenclatures that exist to date. The new transporters discovered occur in diverse bacteria, including Spirochaetes , Bacteroidetes , Planctomycetes and Verrucomicrobia , many of which are species that have not been previously recognized to have sialometabolic capacities. Two subfamilies of transporters stand out in being fused to the sialic acid mutarotase enzyme, NanM, and these transporter fusions are enriched in bacteria present in gut microbial communities. Our analysis supports the increasing experimental evidence that competition for host-derived sialic acid is a key phenotype for successful colonization of complex mucosal microbiomes, such that a strong evolutionary selection has occurred for the emergence of sialic acid specificity within existing transporter architectures.

scholarly journals Hydrogen Does Not Appear To Be a Major Electron Donor for Symbiosis with the Deep-Sea Hydrothermal Vent Tubeworm Riftia pachyptila

2019 ◽  
Vol 86 (1) ◽  
Author(s):  
Jessica H. Mitchell ◽  
Juliana M. Leonard ◽  
Jennifer Delaney ◽  
Peter R. Girguis ◽  
Kathleen M. Scott
Keyword(s):  
High Pressure ◽  
Electron Donor ◽  
Deep Sea ◽  
Symbiotic Association ◽  
Omics Data ◽  
Riftia Pachyptila ◽  
Free Living ◽  
Content Type ◽  
Genes Encoding ◽  
Chemolithoautotrophic Bacteria

ABSTRACT Use of hydrogen gas (H2) as an electron donor is common among free-living chemolithotrophic microorganisms. Given the presence of this dissolved gas at deep-sea hydrothermal vents, it has been suggested that it may also be a major electron donor for the free-living and symbiotic chemolithoautotrophic bacteria that are the primary producers at these sites. Giant Riftia pachyptila siboglinid tubeworms and their symbiotic bacteria (“Candidatus Endoriftia persephone”) dominate many vents in the Eastern Pacific, and their use of sulfide as a major electron donor has been documented. Genes encoding hydrogenase are present in the “Ca. Endoriftia persephone” genome, and proteome data suggest that these genes are expressed. In this study, high-pressure respirometry of intact R. pachyptila and incubations of trophosome homogenate were used to determine whether this symbiotic association could also use H2 as a major electron donor. Measured rates of H2 uptake by intact R. pachyptila in high-pressure respirometers were similar to rates measured in the absence of tubeworms. Oxygen uptake rates in the presence of H2 were always markedly lower than those measured in the presence of sulfide, as was the incorporation of 13C-labeled dissolved inorganic carbon. Carbon fixation by trophosome homogenate was not stimulated by H2, nor was hydrogenase activity detectable in these samples. Though genes encoding [NiFe] group 1e and [NiFe] group 3b hydrogenases are present in the genome and transcribed, it does not appear that H2 is a major electron donor for this system, and it may instead play a role in intracellular redox homeostasis. IMPORTANCE Despite the presence of hydrogenase genes, transcripts, and proteins in the “Ca. Endoriftia persephone” genome, transcriptome, and proteome, it does not appear that R. pachyptila can use H2 as a major electron donor. For many uncultivable microorganisms, omic analyses are the basis for inferences about their activities in situ. However, as is apparent from the study reported here, there are dangers in extrapolating from omics data to function, and it is essential, whenever possible, to verify functions predicted from omics data with physiological and biochemical measurements.

scholarly journals Influences of a Prolific Gut Fungus (Zancudomyces culisetae) on Larval and Adult Mosquito (Aedes aegypti)-Associated Microbiota

2019 ◽  
Vol 86 (3) ◽  
Author(s):  
Jonas Frankel-Bricker ◽  
Sven Buerki ◽  
Kevin P. Feris ◽  
Merlin M. White
Keyword(s):  
Aedes Aegypti ◽  
Developmental Stages ◽  
Whole Body ◽  
Fungal Colonization ◽  
Content Type ◽  
Downstream Effects ◽  
Microbe Interactions ◽  
Transstadial Transmission ◽  
Community Variation ◽  
Host Microbe Interactions

ABSTRACT Adult mosquitoes inherit a bacterial community from larvae via transstadial transmission, an understudied process that may influence host-microbe interactions. Microbes contribute to important host life history traits, and analyzing transmitted microbial communities, the interrelationship between larval and adult-associated microbiota, and factors influencing host-microbe relationships provides targets for research. During its larval stage, the yellow fever mosquito (Aedes aegypti) hosts the trichomycete gut fungus Zancudomyces culisetae, and fungal colonization coincides with environmental perturbations in the digestive tract microecosystem. Natural populations are differentially exposed to fungi, thereby potentially harboring distinct microbiota and experiencing disparate host-microbe interactions. This study’s objectives were to characterize larval and initial adult microbiomes, investigate variation in diversity and distribution of microbial communities across individuals, and assess whether larval fungal colonization impacted microbiomes at these developmental stages. Laboratory-based fungal infestation assays, sequencing of 16S rRNA gene amplicons, and bacterial load quantification protocols revealed that initial adult microbiomes varied in diversity and distribution. Larval fungal colonization had downstream effects on initial adult microbiomes, significantly reducing microbial community variation, shifting relative abundances of certain bacterial families, and influencing transstadial transmission outcomes of particular genera. Further, abundances of several families consistently decreased in adults relative to levels in larvae, possibly reflecting impacts of host development on specific bacterial taxa. These findings demonstrated that a prolific gut fungus impacted mosquito-associated microbiota at two developmental stages in an insect connected with global human health. IMPORTANCE Mosquitoes are widespread vectors of numerous human pathogens and harbor microbiota known to affect host phenotypic traits. However, little research has directly investigated how bacterial communities associated with larvae and adults are connected. We characterized whole-body bacterial communities in mosquito larvae preceding pupation and in newly emerged adults, and investigated whether a significant biotic factor, fungal colonization of the larval hindgut, impacted these microbiomes. Results showed that fungal colonization reduced microbial community variation across individuals and differentially impacted the outcomes of transstadial transmission for certain bacterial genera, revealing downstream effects of the fungus on initial adult microbiomes. The importance of our research is in providing a thorough comparative analysis of whole-body microbiota harbored in larvae and adults of the yellow fever mosquito (Aedes aegypti) and in demonstrating the important role a widespread gut fungus played in a host-associated microbiome.

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 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 Intestinal Epithelial Ecto-5′-Nucleotidase (CD73) Regulates Intestinal Colonization and Infection by Nontyphoidal Salmonella

2017 ◽  
Vol 85 (10) ◽  
Author(s):  
Daniel J. Kao ◽  
Bejan J. Saeedi ◽  
David Kitzenberg ◽  
Krista M. Burney ◽  
Evgenia Dobrinskikh ◽  
...  
Keyword(s):  
Fold Increase ◽  
Apical Surface ◽  
Protective Effects ◽  
Intestinal Epithelial ◽  
Extracellular Adenosine ◽  
Content Type ◽  
Serovar Typhimurium ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Cd73 Expression

ABSTRACT Ecto-5′-nucleotidase (CD73) is expressed abundantly on the apical surface of intestinal epithelial cells (IECs) and functions as the terminal enzyme in the generation of extracellular adenosine. Previous work demonstrated that adenosine signaling in IECs results in a number of tissue-protective effects during inflammation; however, a rationale for its apical expression has been lacking. We hypothesized that the highly polarized expression of CD73 is indicative of an important role for extracellular adenosine as a mediator of host-microbe interactions. We show that adenosine harbors bacteriostatic activity against Salmonella enterica serovar Typhimurium that is not shared by the related purine metabolite 5′-AMP, inosine, or hypoxanthine. Analysis of Salmonella colonization in IEC-specific CD73 knockout mice (CD73 f/f Villin Cre ) revealed a nearly 10-fold increase in colonization compared to that in controls. Despite the increased luminal colonization by Salmonella, CD73 f/f Villin Cre mice were protected against Salmonella colitis and showed reduced Salmonella burdens in viscera, suggesting that adenosine promotes dissemination. The knockdown of CD73 expression in cultured IECs resulted in dramatic defects in intraepithelial localization and replication as well as defective transepithelial translocation by Salmonella. In conclusion, we define a novel antimicrobial activity of adenosine in the gastrointestinal tract and unveil an important role for adenosine as a regulator of host-microbe interactions. These findings have broad implications for the development of new therapeutic agents for infectious disease.

scholarly journals The Lumen of Human Intestinal Organoids Poses Greater Stress to Bacteria Compared to the Germ-Free Mouse Intestine: Escherichia coli Deficient in RpoS as a Colonization Probe

mSphere ◽  
2020 ◽  
Vol 5 (6) ◽  
Author(s):  
Madeline R. Barron ◽  
Roberto J. Cieza ◽  
David R. Hill ◽  
Sha Huang ◽  
Veda K. Yadagiri ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Stress Response ◽  
Content Type ◽  
General Stress Response ◽  
E Coli ◽  
Germ Free ◽  
General Stress ◽  
Microbe Interactions ◽  
Mouse Intestine ◽  
Host Microbe Interactions

ABSTRACT Pluripotent stem-cell-derived human intestinal organoids (HIOs) are three-dimensional, multicellular structures that model a naive intestinal epithelium in an in vitro system. Several published reports have investigated the use of HIOs to study host-microbe interactions. We recently demonstrated that microinjection of the nonpathogenic Escherichia coli strain ECOR2 into HIOs induced morphological and functional maturation of the HIO epithelium, including increased secretion of mucins and cationic antimicrobial peptides. In the current work, we use ECOR2 as a biological probe to further characterize the environment present in the HIO lumen. We generated an isogenic mutant in the general stress response sigma factor RpoS and employed this mutant to compare challenges faced by a bacterium during colonization of the HIO lumen relative to the germ-free mouse intestine. We demonstrate that the loss of RpoS significantly decreases the ability of ECOR2 to colonize HIOs, although it does not prevent colonization of germ-free mice. These results indicate that the HIO lumen is a more restrictive environment to E. coli than the germ-free mouse intestine, thus increasing our understanding of the HIO model system as it pertains to studying the establishment of intestinal host-microbe symbioses. IMPORTANCE Technological advancements have driven and will continue to drive the adoption of organotypic systems for investigating host-microbe interactions within the human intestinal ecosystem. Using E. coli deficient in the RpoS-mediated general stress response, we demonstrate that the type or severity of microbial stressors within the HIO lumen is more restrictive than those of the in vivo environment of the germ-free mouse gut. This study provides important insight into the nature of the HIO microenvironment from a microbiological standpoint.

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