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      Intestinal lysozyme1 deficiency alters microbiota composition and impacts host metabolism through the emergence of NAD +-secreting ASTB Qing110 bacteria

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          ABSTRACT

          The intestine plays a pivotal role in nutrient absorption and host defense against pathogens, orchestrated in part by antimicrobial peptides secreted by Paneth cells. Among these peptides, lysozyme has multifaceted functions beyond its bactericidal activity. Here, we uncover the intricate relationship between intestinal lysozyme, the gut microbiota, and host metabolism. Lysozyme deficiency in mice led to altered body weight, energy expenditure, and substrate utilization, particularly on a high-fat diet. Interestingly, these metabolic benefits were linked to changes in the gut microbiota composition. Cohousing experiments revealed that the metabolic effects of lysozyme deficiency were microbiota-dependent. 16S rDNA sequencing highlighted differences in microbial communities, with ASTB_g (OTU60) highly enriched in lysozyme knockout mice. Subsequently, a novel bacterium, ASTB Qing110, corresponding to ASTB_g (OTU60), was isolated. Metabolomic analysis revealed that ASTB Qing110 secreted high levels of NAD +, potentially influencing host metabolism. This study sheds light on the complex interplay between intestinal lysozyme, the gut microbiota, and host metabolism, uncovering the potential role of ASTB Qing110 as a key player in modulating metabolic outcomes.

          IMPORTANCE

          The impact of intestinal lumen lysozyme on intestinal health is complex, arising from its multifaceted interactions with the gut microbiota. Lysozyme can both mitigate and worsen certain health conditions, varying with different scenarios. This underscores the necessity of identifying the specific bacterial responses elicited by lysozyme and understanding their molecular foundations. Our research reveals that a deficiency in intestinal lysozyme1 may offer protection against diet-induced obesity by altering bacterial populations. We discovered a strain of bacterium, ASTB Qing110, which secretes NAD + and is predominantly found in lyz1-deficient mice. Qing110 demonstrates positive effects in both C. elegans and mouse models of ataxia telangiectasia. This study sheds light on the intricate role of lysozyme in influencing intestinal health.

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          Most cited references59

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          The Hallmarks of Aging

          Aging is characterized by a progressive loss of physiological integrity, leading to impaired function and increased vulnerability to death. This deterioration is the primary risk factor for major human pathologies, including cancer, diabetes, cardiovascular disorders, and neurodegenerative diseases. Aging research has experienced an unprecedented advance over recent years, particularly with the discovery that the rate of aging is controlled, at least to some extent, by genetic pathways and biochemical processes conserved in evolution. This Review enumerates nine tentative hallmarks that represent common denominators of aging in different organisms, with special emphasis on mammalian aging. These hallmarks are: genomic instability, telomere attrition, epigenetic alterations, loss of proteostasis, deregulated nutrient sensing, mitochondrial dysfunction, cellular senescence, stem cell exhaustion, and altered intercellular communication. A major challenge is to dissect the interconnectedness between the candidate hallmarks and their relative contributions to aging, with the final goal of identifying pharmaceutical targets to improve human health during aging, with minimal side effects. Copyright © 2013 Elsevier Inc. All rights reserved.
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            THE GENETICS OF CAENORHABDITIS ELEGANS

            Methods are described for the isolation, complementation and mapping of mutants of Caenorhabditis elegans, a small free-living nematode worm. About 300 EMS-induced mutants affecting behavior and morphology have been characterized and about one hundred genes have been defined. Mutations in 77 of these alter the movement of the animal. Estimates of the induced mutation frequency of both the visible mutants and X chromosome lethals suggests that, just as in Drosophila, the genetic units in C.elegans are large.
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              Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies

              The recent advent of DNA sequencing technologies facilitates the use of genome sequencing data that provide means for more informative and precise classification and identification of members of the Bacteria and Archaea. Because the current species definition is based on the comparison of genome sequences between type and other strains in a given species, building a genome database with correct taxonomic information is of paramount need to enhance our efforts in exploring prokaryotic diversity and discovering novel species as well as for routine identifications. Here we introduce an integrated database, called EzBioCloud, that holds the taxonomic hierarchy of the Bacteria and Archaea, which is represented by quality-controlled 16S rRNA gene and genome sequences. Whole-genome assemblies in the NCBI Assembly Database were screened for low quality and subjected to a composite identification bioinformatics pipeline that employs gene-based searches followed by the calculation of average nucleotide identity. As a result, the database is made of 61 700 species/phylotypes, including 13 132 with validly published names, and 62 362 whole-genome assemblies that were identified taxonomically at the genus, species and subspecies levels. Genomic properties, such as genome size and DNA G+C content, and the occurrence in human microbiome data were calculated for each genus or higher taxa. This united database of taxonomy, 16S rRNA gene and genome sequences, with accompanying bioinformatics tools, should accelerate genome-based classification and identification of members of the Bacteria and Archaea. The database and related search tools are available at www.ezbiocloud.net/.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review and editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draft
                Role: Data curationRole: MethodologyRole: SoftwareRole: Writing – review and editing
                Role: Editor
                Journal
                mSystems
                mSystems
                msystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                March 2024
                16 February 2024
                16 February 2024
                : 9
                : 3
                : e01214-23
                Affiliations
                [1 ]Institute for Immunology, School of Medicine, Tsinghua University; , Beijing, China
                [2 ]Beijing Institute of Genomics, Chinese Academy of Sciences, China National Center for Bioinformation; , Beijing, China
                [3 ]University of Chinese Academy of Sciences; , Beijing, China
                [4 ]Tsinghua-Peking Center for Life Sciences, Tsinghua University; , Beijing, China
                Southern Medical University; , Guangzhou, China
                Author notes
                Address correspondence to Zhihua Liu, zhihualiu@ 123456mail.tsinghua.edu.cn

                Chengye Zhang and Chen Xiang contributed equally to this article. Author order was determined by tossing a coin.

                The authors declare no conflict of interest.

                Author information
                https://orcid.org/0009-0004-3628-7936
                https://orcid.org/0000-0002-0269-0901
                Article
                01214-23 msystems.01214-23
                10.1128/msystems.01214-23
                10949482
                38364095
                39a0ee37-e352-4ed6-958c-2c802a45f5a6
                Copyright © 2024 Zhang et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 14 November 2023
                : 26 January 2024
                Page count
                supplementary-material: 2, authors: 9, Figures: 5, References: 61, Pages: 22, Words: 12871
                Funding
                Funded by: MOST | National Key Research and Development Program of China (NKPs);
                Award ID: 2017YFA0503403, 2018YFE0207300
                Award Recipient :
                Funded by: MOST | National Natural Science Foundation of China (NSFC);
                Award ID: 31730028
                Award Recipient :
                Categories
                Research Article
                open-peer-review, Open Peer Review
                host-microbial-interactions, Host-Microbial Interactions
                Custom metadata
                March 2024

                lyz1,gut microbiota,metabolism,nad+,aging
                lyz1, gut microbiota, metabolism, nad+, aging

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