Blog
About

7
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Monoassociation with Lactobacillus plantarum Disrupts Intestinal Homeostasis in Adult Drosophila melanogaster

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          ABSTRACT

          Adult Drosophila melanogaster raised in the absence of symbiotic bacteria have fewer intestinal stem cell divisions and a longer life span than their conventionally reared counterparts. However, we do not know if increased stem cell divisions are essential for symbiont-dependent regulation of longevity. To determine if individual symbionts cause aging-dependent death in Drosophila, we examined the impacts of common symbionts on host longevity. We found that monoassociation of adult Drosophila with Lactobacillus plantarum, a widely reported fly symbiont and member of the probiotic Lactobacillus genus, curtails adult longevity relative to germfree counterparts. The effects of Lactobacillus plantarum on life span were independent of intestinal aging. Instead, we found that association with Lactobacillus plantarum causes an extensive intestinal pathology within the host, characterized by loss of stem cells, impaired epithelial renewal, and a gradual erosion of epithelial ultrastructure. Our study uncovers an unknown aspect of Lactobacillus plantarum- Drosophila interactions and establishes a simple model to characterize symbiont-dependent disruption of intestinal homeostasis.

          IMPORTANCE

          Under homeostatic conditions, gut bacteria provide molecular signals that support the organization and function of the host intestine. Sudden shifts in the composition or distribution of gut bacterial communities impact host receipt of bacterial cues and disrupt tightly regulated homeostatic networks. We used the Drosophila melanogaster model to determine the effects of prominent fly symbionts on host longevity and intestinal homeostasis. We found that monoassociation with Lactobacillus plantarum leads to a loss of intestinal progenitor cells, impaired epithelial renewal, and disruption of gut architecture as flies age. These observations uncover a novel phenotype caused by monoassociation of a germfree host with a common symbiont and establish a simple model to characterize symbiont-dependent loss of intestinal homeostasis.

          Related collections

          Most cited references 51

          • Record: found
          • Abstract: not found
          • Article: not found

          Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.

            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut.

            Cells in intestinal epithelia turn over rapidly due to damage from digestion and toxins produced by the enteric microbiota. Gut homeostasis is maintained by intestinal stem cells (ISCs) that divide to replenish the intestinal epithelium, but little is known about how ISC division and differentiation are coordinated with epithelial cell loss. We show here that when enterocytes (ECs) in the Drosophila midgut are subjected to apoptosis, enteric infection, or JNK-mediated stress signaling, they produce cytokines (Upd, Upd2, and Upd3) that activate Jak/Stat signaling in ISCs, promoting their rapid division. Upd/Jak/Stat activity also promotes progenitor cell differentiation, in part by stimulating Delta/Notch signaling, and is required for differentiation in both normal and regenerating midguts. Hence, cytokine-mediated feedback enables stem cells to replace spent progeny as they are lost, thereby establishing gut homeostasis.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling.

              The symbiotic microbiota profoundly affect many aspects of host physiology; however, the molecular mechanisms underlying host-microbe cross-talk are largely unknown. Here, we show that the pyrroloquinoline quinone-dependent alcohol dehydrogenase (PQQ-ADH) activity of a commensal bacterium, Acetobacter pomorum, modulates insulin/insulin-like growth factor signaling (IIS) in Drosophila to regulate host homeostatic programs controlling developmental rate, body size, energy metabolism, and intestinal stem cell activity. Germ-free animals monoassociated with PQQ-ADH mutant bacteria displayed severe deregulation of developmental and metabolic homeostasis. Importantly, these defects were reversed by enhancing host IIS or by supplementing the diet with acetic acid, the metabolic product of PQQ-ADH.
                Bookmark

                Author and article information

                Contributors
                Role: Editor
                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                31 July 2018
                Jul-Aug 2018
                : 9
                : 4
                Affiliations
                [a ]Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, Alberta, Canada
                Max Planck Institute for Marine Microbiology
                Author notes
                Address correspondence to Edan Foley, efoley@ 123456ualberta.ca .
                Article
                mBio01114-18
                10.1128/mBio.01114-18
                6069112
                30065090
                Copyright © 2018 Fast et al.

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

                Page count
                supplementary-material: 1, Figures: 6, Tables: 0, Equations: 0, References: 65, Pages: 16, Words: 8964
                Product
                Funding
                Funded by: Canadian Institutes of Health Research;
                Award ID: MOP77746
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                July/August 2018

                Life sciences

                symbionts, drosophila, lactobacillus, epithelial cells, host response, stem cells

                Comments

                Comment on this article