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Gut Microbiota in Immunity and Inflammatory Diseases

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A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cellular Immunology".

Deadline for manuscript submissions: closed (1 November 2020) | Viewed by 58913

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Special Issue Editors

Dr. Miloslav Kverka

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Guest Editor

Institute of Microbiology of the Academy of Sciences of the Czech Republic, Prague, Czech Republic
Interests: mucosal immunology; host–microbe interactions; inflammatory diseases; biomarker research

Dr. Klára Kostovčíková

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Guest Editor

Institute of Microbiology of the Academy of Sciences of the Czech Republic, Prague, Czech Republic
Interests: mucosal immunology; host-microbe interactions; inflammatory diseases; cancer; microbial metabolites

Special Issue Information

Dear Colleagues,

In humans, gut microbiota represent a complex ecosystem that consists of bacteria, Archaea, fungi, parasites, and an ill-defined number of viruses, mostly bacteriophages. Studies in gnotobionts (i.e., germ-free or artificially colonized animals) have clearly shown that without this complex ecosystem, the immune system and many other physiological functions would never reach their full potential. While niche specificities and initial environmental microbiota are crucial for early microbial colonization, it may later be significantly influenced by diet or antibiotics with consequences for the individual’s health. Changes in diet drive microbes to adapt to a new substrate, thus inducing profound changes in microbiota that could improve the host’s ability to adapt to the environment. These adaptive changes are similar across different mammalian lineages and have important implications for the host’s health. Several inflammatory diseases are linked to gut microbiota dysbiosis, i.e., changes in microbiota composition or function. The most studied is its effect on diseases affecting gut and metabolic diseases, but perturbations in gut microbiota could also affect extra-intestinal inflammation by promoting shifts in the immune system reactivity. With this Special Issue, we aim to provide an overview of the recent advances in the research of host–microbe interactions and their consequences for the immune system and health in general. Moreover, we would like to discuss these issues from another point of view: how the host’s immune system and environmental factors influence this complex ecosystem. Finally, with this in mind, we would like to focus on all members of gut microbial niche (i.e., bacteria, Archea, fungi, viruses and parasites) with an emphasis on new mechanisms and new avenues for immunomodulatory interventions.

Dr. Miloslav Kverka
Dr. Klára Kostovčíková
Guest Editors

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Keywords

gut microbiota
inflammation
dysbiosis
probiotics
host-microbe interactions

Published Papers (12 papers)

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Research

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19 pages, 3704 KiB

Open AccessFeature PaperArticle

Severity of Experimental Autoimmune Uveitis Is Reduced by Pretreatment with Live Probiotic Escherichia coli Nissle 1917

by Otakar Dusek, Alena Fajstova, Aneta Klimova, Petra Svozilkova, Tomas Hrncir, Miloslav Kverka, Stepan Coufal, Johan Slemin, Helena Tlaskalova-Hogenova, John V. Forrester and Jarmila Heissigerova

Cells 2021, 10(1), 23; https://doi.org/10.3390/cells10010023 - 25 Dec 2020

Cited by 13 | Viewed by 3553

Abstract

Non-infectious uveitis is considered an autoimmune disease responsible for a significant burden of blindness in developed countries and recent studies have linked its pathogenesis to dysregulation of the gut microbiota. We tested the immunomodulatory properties of two probiotics, Escherichia coli Nissle 1917 (EcN) and E. coli O83:K24:H31 (EcO), in a model of experimental autoimmune uveitis (EAU). To determine the importance of bacterial viability and treatment timing, mice were orally treated with live or autoclaved bacteria in both preventive and therapeutic schedules. Disease severity was assessed by ophthalmoscopy and histology, immune phenotypes in mesenteric and cervical lymph nodes were analyzed by flow cytometry and the gut immune environment was analyzed by RT-PCR and/or gut tissue culture. EcN, but not EcO, protected against EAU but only as a live organism and only when administered before or at the time of disease induction. Successful prevention of EAU was accompanied by a decrease in IRBP-specific T cell response in the lymph nodes draining the site of immunization as early as 7 days after the immunization and eye-draining cervical lymph nodes when the eye inflammation became apparent. Furthermore, EcN promoted an anti-inflammatory response in Peyer’s patches, increased gut antimicrobial peptide expression and decreased production of inducible nitric oxide synthase in macrophages. In summary, we show here that EcN controls inflammation in EAU and suggest that probiotics may have a role in regulating the gut–eye axis. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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24 pages, 3904 KiB

Open AccessArticle

Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling

by Alena Fajstova, Natalie Galanova, Stepan Coufal, Jana Malkova, Martin Kostovcik, Martina Cermakova, Helena Pelantova, Marek Kuzma, Blanka Sediva, Tomas Hudcovic, Tomas Hrncir, Helena Tlaskalova-Hogenova, Miloslav Kverka and Klara Kostovcikova

Cells 2020, 9(12), 2701; https://doi.org/10.3390/cells9122701 - 16 Dec 2020

Cited by 40 | Viewed by 5928

Abstract

Diet is a strong modifier of microbiome and mucosal microenvironment in the gut. Recently, components of western-type diets have been associated with metabolic and immune diseases. Here, we studied how high-sugar diet (HSD) consumption influences gut mucosal barrier and immune response under steady state conditions and in a mouse model of acute colitis. We found that HSD significantly increased gut permeability, spleen weight, and neutrophil levels in spleens of healthy mice. Subsequent dextran sodium sulfate administration led to severe colitis. In colon, HSD significantly promoted neutrophil infiltration and increased the levels of IL-6, IL-1β, and TNF-α. Moreover, HSD-fed mice had significantly higher abundance of pathobionts, such as Escherichia coli and Candida, in fecal samples. Although germ-free mice colonized with microbiota of conventionally reared mice that consumed different diets had equally severe colitis, mice colonized with HSD microbiota showed markedly increased infiltration of neutrophils to the gut. The induction of colitis in Toll-like receptor 4 (TLR4)-deficient HSD-fed mice led to significantly milder colitis than in wild-type mice. In conclusion, our results suggested a significant role of HSD in disruption of barrier integrity and balanced mucosal and systemic immune response. In addition, these processes seemed to be highly influenced by resident potentially pathogenic microbiota or metabolites via the TLR4 signaling pathway. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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18 pages, 2017 KiB

Open AccessArticle

Gut Microbiome Changes in Patients with Active Left-Sided Ulcerative Colitis after Fecal Microbiome Transplantation and Topical 5-aminosalicylic Acid Therapy

by Dagmar Schierová, Jan Březina, Jakub Mrázek, Kateřina Olša Fliegerová, Simona Kvasnová, Lukáš Bajer and Pavel Drastich

Cells 2020, 9(10), 2283; https://doi.org/10.3390/cells9102283 - 13 Oct 2020

Cited by 36 | Viewed by 4003

Abstract

Ulcerative colitis (UC) is an inflammatory bowel disease, and intestinal bacteria are implicated in the pathogenesis of this disorder. The administration of aminosalicylates (5-ASA) is a conventional treatment that targets the mucosa, while fecal microbial transplantation (FMT) is a novel treatment that directly targets the gut microbiota. The aim of this study was to identify changes in fecal bacterial composition after both types of treatments and evaluate clinical responses. Sixteen patients with active left-sided UC underwent enema treatment using 5-ASA (n = 8) or FMT (n = 8) with a stool from a single donor. Fecal microbiota were analyzed by 16S rDNA high-throughput sequencing, and clinical indices were used to assess the efficacy of treatments. 5-ASA therapy resulted in clinical remission in 50% (4/8) of patients, but no correlation with changes in fecal bacteria was observed. In FMT, remission was achieved in 37.5% (3/8) of patients and was associated with a significantly increased relative abundance of the families Lachnospiraceae, Ruminococcaceae, and Clostridiaceae of the phylum Firmicutes, and Bifidobacteriaceae and Coriobacteriaceae of the phylum Actinobacteria. At the genus level, Faecalibacterium, Blautia, Coriobacteria, Collinsela, Slackia, and Bifidobacterium were significantly more frequent in patients who reached clinical remission. However, the increased abundance of beneficial taxa was not a sufficient factor to achieve clinical improvement in all UC patients. Nevertheless, our preliminary results indicate that FMT as non-drug-using method is thought to be a promising treatment for UC patients. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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22 pages, 5428 KiB

Open AccessArticle

In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of Parabacteroides distasonis Strains Alleviating TNBS-Induced Colitis in Mice

by Bernardo Cuffaro, Aka L. W. Assohoun, Denise Boutillier, Lenka Súkeníková, Jérémy Desramaut, Samira Boudebbouze, Sophie Salomé-Desnoulez, Jiří Hrdý, Anne-Judith Waligora-Dupriet, Emmanuelle Maguin and Corinne Grangette

Cells 2020, 9(9), 2104; https://doi.org/10.3390/cells9092104 - 16 Sep 2020

Cited by 41 | Viewed by 4766

Abstract

Alterations in the gut microbiota composition and diversity seem to play a role in the development of chronic diseases, including inflammatory bowel disease (IBD), leading to gut barrier disruption and induction of proinflammatory immune responses. This opens the door for the use of novel health-promoting bacteria. We selected five Parabacteroides distasonis strains isolated from human adult and neonates gut microbiota. We evaluated in vitro their immunomodulation capacities and their ability to reinforce the gut barrier and characterized in vivo their protective effects in an acute murine model of colitis. The in vitro beneficial activities were highly strain dependent: two strains exhibited a potent anti-inflammatory potential and restored the gut barrier while a third strain reinstated the epithelial barrier. While their survival to in vitro gastric conditions was variable, the levels of P. distasonis DNA were higher in the stools of bacteria-treated animals. The strains that were positively scored in vitro displayed a strong ability to rescue mice from colitis. We further showed that two strains primed dendritic cells to induce regulatory T lymphocytes from naïve CD4⁺ T cells. This study provides better insights on the functionality of commensal bacteria and crucial clues to design live biotherapeutics able to target inflammatory chronic diseases such as IBD. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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14 pages, 1424 KiB

Open AccessArticle

In Silico Evaluation of Putative S100B Interacting Proteins in Healthy and IBD Gut Microbiota

by Massimiliano Orsini, Rosa Di Liddo, Federica Valeriani, Marzia Mancin, Renata D’Incà, Andrea Castagnetti, Antonio Aceti, Pier Paolo Parnigotto, Vincenzo Romano Spica and Fabrizio Michetti

Cells 2020, 9(7), 1697; https://doi.org/10.3390/cells9071697 - 15 Jul 2020

Cited by 9 | Viewed by 2925

Abstract

The crosstalk between human gut microbiota and intestinal wall is essential for the organ’s homeostasis and immune tolerance. The gut microbiota plays a role in healthy and pathological conditions mediated by inflammatory processes or by the gut-brain axes, both involving a possible role for S100B protein as a diffusible cytokine present not only in intestinal mucosa but also in faeces. In order to identify target proteins for a putative interaction between S100B and the microbiota proteome, we developed a bioinformatics workflow by integrating the interaction features of known domains with the proteomics data derived from metataxonomic studies of the gut microbiota from healthy and inflammatory bowel disease (IBD) subjects. On the basis of the microbiota composition, proteins putatively interacting with S100B domains were in fact found, both in healthy subjects and IBD patients, in a reduced number in the latter samples, also exhibiting differences in interacting domains occurrence between the two groups. In addition, differences between ulcerative colitis and Crohn disease samples were observed. These results offer the conceptual framework for where to investigate the role of S100B as a candidate signalling molecule in the microbiota/gut communication machinery, on the basis of interactions differently conditioned by healthy or pathological microbiota. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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20 pages, 4096 KiB

Open AccessFeature PaperArticle

The Bioinformatic and In Vitro Studies of Clostridioides Difficile Aminopeptidase M24 Revealed the Immunoreactive KKGIK Peptide

by Katarzyna Pacyga, Agnieszka Razim, Gayane Martirosian, Małgorzata Aptekorz, Andrzej Szuba, Andrzej Gamian, Andrzej Myc and Sabina Górska

Cells 2020, 9(5), 1146; https://doi.org/10.3390/cells9051146 - 07 May 2020

Cited by 2 | Viewed by 2734

Abstract

Clostridioides difficile (CD) is a Gram-positive pathogen responsible for CD-associated disease (CDAD), which is characterized by symptoms ranging from mild diarrhea to pseudomembranous colitis. This work is an attempt to respond to the need of novel methods for CD infection (CDI) prevention, since the number of CDI cases is still rising. A bioinformatics approach was applied to design twenty-one peptides consisting of in silico predicted linear B-cell and T-cell epitopes of aminopeptidase M24 from CD. These peptides were mapped for epitopes exploiting PEPSCAN procedure and using sera obtained from CD infected patients, umbilical cord blood, and healthy volunteers. Two new CD epitopes, ¹³¹KKGIK¹³⁵ and ¹⁸⁴KGTSTHVIT¹⁹², were identified and characterized. Immunoreactivity of the synthetic biotinylated ¹³¹KKGIK¹³⁵ epitope was significantly higher compared to ¹⁸⁴KGTSTHVIT¹⁹² epitope in Enzyme-Linked Immunosorbent Assay (ELISA) with umbilical cord blood and CDI patients’ sera. Hereafter, the conjugate of bovine serum albumin and epitope ¹³¹KKGIK¹³⁵ was evaluated in vitro on lung epithelial cell line. In vitro, a significant induction of IL-6 by conjugate was observed, thereby we postulate that this new ¹³¹KKGIK¹³⁵ epitope possesses immunostimulating properties suggesting possibility of its use in a vaccine against Clostridioides difficile. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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22 pages, 4225 KiB

Open AccessFeature PaperArticle

A Commercial Probiotic Induces Tolerogenic and Reduces Pathogenic Responses in Experimental Autoimmune Encephalomyelitis

by Laura Calvo-Barreiro, Herena Eixarch, Manuel Ponce-Alonso, Mireia Castillo, Rafael Lebrón-Galán, Leyre Mestre, Carmen Guaza, Diego Clemente, Rosa del Campo, Xavier Montalban and Carmen Espejo

Cells 2020, 9(4), 906; https://doi.org/10.3390/cells9040906 - 07 Apr 2020

Cited by 30 | Viewed by 5909

Abstract

Previous studies in experimental autoimmune encephalomyelitis (EAE) models have shown that some probiotic bacteria beneficially impact the development of this experimental disease. Here, we tested the therapeutic effect of two commercial multispecies probiotics—Lactibiane iki and Vivomixx—on the clinical outcome of established EAE. Lactibiane iki improves EAE clinical outcome in a dose-dependent manner and decreases central nervous system (CNS) demyelination and inflammation. This clinical improvement is related to the inhibition of pro-inflammatory and the stimulation of immunoregulatory mechanisms in the periphery. Moreover, both probiotics modulate the number and phenotype of dendritic cells (DCs). Specifically, Lactibiane iki promotes an immature, tolerogenic phenotype of DCs that can directly induce immune tolerance in the periphery, while Vivomixx decreases the percentage of DCs expressing co-stimulatory molecules. Finally, gut microbiome analysis reveals an altered microbiome composition related to clinical condition and disease progression. This is the first preclinical assay that demonstrates that a commercial probiotic performs a beneficial and dose-dependent effect in EAE mice and one of the few that demonstrates a therapeutic effect once the experimental disease is established. Because this probiotic is already available for clinical trials, further studies are being planned to explore its therapeutic potential in multiple sclerosis patients. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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20 pages, 4199 KiB

Open AccessArticle

Lactobacillus fermentum CECT5716 Supplementation in Rats during Pregnancy and Lactation Impacts Maternal and Offspring Lipid Profile, Immune System and Microbiota

by Ignasi Azagra-Boronat, Alba Tres, Malén Massot-Cladera, Àngels Franch, Margarida Castell, Francesc Guardiola, Francisco J. Pérez-Cano and Maria J. Rodríguez-Lagunas

Cells 2020, 9(3), 575; https://doi.org/10.3390/cells9030575 - 28 Feb 2020

Cited by 21 | Viewed by 3553

Abstract

Probiotics have shown potential for their use in early life. This study aimed to investigate whether the administration of Lactobacillus fermentum CECT5716 during pregnancy and lactation periods impacts maternal and offspring plasma lipid profile, immune system and microbiota. Rats were supplemented with the probiotic during gestation and two weeks of lactation. After supplementation, although the microbiota composition was not affected, the probiotic strain was detected in all cecal contents of dams and in some of their pups. Dams showed reduced proportion of T cytotoxic cells in the mesenteric lymph nodes, modulation of intestinal cytokines (IL-10 and IL-12) and changes in plasma fatty acids (20:0, 22:0, 20:5 n-3, and 18:3 n-6). Pups showed changes in immunoglobulins (intestinal IgA and plasmatic IgG2a and IgG2c) and fatty acid profile (17:0, 22:0, and 18:2 n-6). Overall, Lactobacillus fermentum CECT5716 supplementation contributed to beneficially modulating the immune system of the mother and its offspring. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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Review

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28 pages, 2465 KiB

Open AccessReview

Complex Interaction between Resident Microbiota and Misfolded Proteins: Role in Neuroinflammation and Neurodegeneration

by Juliana González-Sanmiguel, Christina M. A. P. Schuh, Carola Muñoz-Montesino, Pamina Contreras-Kallens, Luis G. Aguayo and Sebastian Aguayo

Cells 2020, 9(11), 2476; https://doi.org/10.3390/cells9112476 - 13 Nov 2020

Cited by 28 | Viewed by 5395

Abstract

Neurodegenerative diseases such as Alzheimer’s disease (AD), Parkinson’s disease (PD) and Creutzfeldt–Jakob disease (CJD) are brain conditions affecting millions of people worldwide. These diseases are associated with the presence of amyloid-β (Aβ), alpha synuclein (α-Syn) and prion protein (PrP) depositions in the brain, respectively, which lead to synaptic disconnection and subsequent progressive neuronal death. Although considerable progress has been made in elucidating the pathogenesis of these diseases, the specific mechanisms of their origins remain largely unknown. A body of research suggests a potential association between host microbiota, neuroinflammation and dementia, either directly due to bacterial brain invasion because of barrier leakage and production of toxins and inflammation, or indirectly by modulating the immune response. In the present review, we focus on the emerging topics of neuroinflammation and the association between components of the human microbiota and the deposition of Aβ, α-Syn and PrP in the brain. Special focus is given to gut and oral bacteria and biofilms and to the potential mechanisms associating microbiome dysbiosis and toxin production with neurodegeneration. The roles of neuroinflammation, protein misfolding and cellular mediators in membrane damage and increased permeability are also discussed. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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25 pages, 3021 KiB

Open AccessReview

The Microbiota and Gut-Related Disorders: Insights from Animal Models

by Layla Kamareddine, Hoda Najjar, Muhammad Umar Sohail, Hadil Abdulkader and Maha Al-Asmakh

Cells 2020, 9(11), 2401; https://doi.org/10.3390/cells9112401 - 02 Nov 2020

Cited by 19 | Viewed by 4177

Abstract

Over the past decade, the scientific committee has called for broadening our horizons in understanding host–microbe interactions and infectious disease progression. Owing to the fact that the human gut harbors trillions of microbes that exhibit various roles including the production of vitamins, absorption of nutrients, pathogen displacement, and development of the host immune system, particular attention has been given to the use of germ-free (GF) animal models in unraveling the effect of the gut microbiota on the physiology and pathophysiology of the host. In this review, we discuss common methods used to generate GF fruit fly, zebrafish, and mice model systems and highlight the use of these GF model organisms in addressing the role of gut-microbiota in gut-related disorders (metabolic diseases, inflammatory bowel disease, and cancer), and in activating host defense mechanisms and amending pathogenic virulence. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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16 pages, 2769 KiB

Open AccessReview

Phages and Their Role in Gastrointestinal Disease: Focus on Inflammatory Bowel Disease

by Martin Maronek, Rene Link, Lubos Ambro and Roman Gardlik

Cells 2020, 9(4), 1013; https://doi.org/10.3390/cells9041013 - 18 Apr 2020

Cited by 32 | Viewed by 5025

Abstract

Inflammatory bowel diseases (IBDs) are a group of chronic autoinflammatory diseases including Crohn’s disease and ulcerative colitis. Although the molecular mechanisms governing the pathogenesis of gastrointestinal inflammation are not completely clear, the main factors are presumed to be genetic predisposition, environmental exposure, and the intestinal microbiome. Hitherto, most of the studies focusing on the role of the microbiome studied the action and effect of bacteria. However, the intestinal microbiome comprises other members of the microbial community as well, namely, fungi, protozoa, and viruses. We believe that bacteriophages are among the main orchestrators of the effect of microbiota on the gut mucosa. Therefore, this review aims to summarize the knowledge of the role of intestinal phageome in IBD and to discuss the concept of phage therapy and its future applications. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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16 pages, 2250 KiB

Open AccessReview

Recent Advances in Metabolic Pathways of Sulfate Reduction in Intestinal Bacteria

by Ivan Kushkevych, Jiří Cejnar, Jakub Treml, Dani Dordević, Peter Kollar and Monika Vítězová

Cells 2020, 9(3), 698; https://doi.org/10.3390/cells9030698 - 12 Mar 2020

Cited by 89 | Viewed by 9592

Abstract

Sulfate is present in foods, beverages, and drinking water. Its reduction and concentration in the gut depend on the intestinal microbiome activity, especially sulfate-reducing bacteria (SRB), which can be involved in inflammatory bowel disease (IBD). Assimilatory sulfate reduction (ASR) is present in all living organisms. In this process, sulfate is reduced to hydrogen sulfide and then included in cysteine and methionine biosynthesis. In contrast to assimilatory sulfate reduction, the dissimilatory process is typical for SRB. A terminal product of this metabolism pathway is hydrogen sulfide, which can be involved in gut inflammation and also causes problems in industries (due to corrosion effects). The aim of the review was to compare assimilatory and dissimilatory sulfate reduction (DSR). These processes occur in some species of intestinal bacteria (e.g., Escherichia and Desulfovibrio genera). The main attention was focused on the description of genes and their location in selected strains. Their coding expression of the enzymes is associated with anabolic processes in various intestinal bacteria. These analyzed recent advances can be important factors for proposing possibilities of metabolic pathway extension from hydrogen sulfide to cysteine in intestinal SRB. The switch from the DSR metabolic pathway to the ASR metabolic pathway is important since toxic sulfide is not produced as a final product. Full article

(This article belongs to the Special Issue Gut Microbiota in Immunity and Inflammatory Diseases)

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