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      Impact and Influence of the Natural Vibrio-Squid Symbiosis in Understanding Bacterial–Animal Interactions

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          Abstract

          Animals are colonized by bacteria, and in many cases partners have co-evolved to perform mutually beneficial functions. An exciting and ongoing legacy of the past decade has been an expansion of technology to enable study of natural associations in situ/ in vivo. As a result, more symbioses are being examined, and additional details are being revealed for well-studied systems with a focus on the interactions between partners in the native context. With this framing, we review recent literature from the Vibrio fischeriEuprymna scolopes symbiosis and focus on key studies that have had an impact on understanding bacteria–animal interactions broadly. This is not intended to be a comprehensive review of the system, but rather to focus on particular studies that have excelled at moving from pattern to process in facilitating an understanding of the molecular basis to intriguing observations in the field of host–microbe interactions. In this review we discuss the following topics: processes regulating strain and species specificity; bacterial signaling to host morphogenesis; multiple roles for nitric oxide; flagellar motility and chemotaxis; and efforts to understand unannotated and poorly annotated genes. Overall these studies demonstrate how functional approaches in vivo in a tractable system have provided valuable insight into general principles of microbe–host interactions.

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          Most cited references77

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          A microbial symbiosis factor prevents intestinal inflammatory disease.

          Humans are colonized by multitudes of commensal organisms representing members of five of the six kingdoms of life; however, our gastrointestinal tract provides residence to both beneficial and potentially pathogenic microorganisms. Imbalances in the composition of the bacterial microbiota, known as dysbiosis, are postulated to be a major factor in human disorders such as inflammatory bowel disease. We report here that the prominent human symbiont Bacteroides fragilis protects animals from experimental colitis induced by Helicobacter hepaticus, a commensal bacterium with pathogenic potential. This beneficial activity requires a single microbial molecule (polysaccharide A, PSA). In animals harbouring B. fragilis not expressing PSA, H. hepaticus colonization leads to disease and pro-inflammatory cytokine production in colonic tissues. Purified PSA administered to animals is required to suppress pro-inflammatory interleukin-17 production by intestinal immune cells and also inhibits in vitro reactions in cell cultures. Furthermore, PSA protects from inflammatory disease through a functional requirement for interleukin-10-producing CD4+ T cells. These results show that molecules of the bacterial microbiota can mediate the critical balance between health and disease. Harnessing the immunomodulatory capacity of symbiosis factors such as PSA might potentially provide therapeutics for human inflammatory disorders on the basis of entirely novel biological principles.
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            Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants

            Alternative oxidase (AOX) is a non-energy conserving terminal oxidase in the plant mitochondrial electron transport chain. While respiratory carbon oxidation pathways, electron transport, and ATP turnover are tightly coupled processes, AOX provides a means to relax this coupling, thus providing a degree of metabolic homeostasis to carbon and energy metabolism. Beside their role in primary metabolism, plant mitochondria also act as “signaling organelles”, able to influence processes such as nuclear gene expression. AOX activity can control the level of potential mitochondrial signaling molecules such as superoxide, nitric oxide and important redox couples. In this way, AOX also provides a degree of signaling homeostasis to the organelle. Evidence suggests that AOX function in metabolic and signaling homeostasis is particularly important during stress. These include abiotic stresses such as low temperature, drought, and nutrient deficiency, as well as biotic stresses such as bacterial infection. This review provides an introduction to the genetic and biochemical control of AOX respiration, as well as providing generalized examples of how AOX activity can provide metabolic and signaling homeostasis. This review also examines abiotic and biotic stresses in which AOX respiration has been critically evaluated, and considers the overall role of AOX in growth and stress tolerance.
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              Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures.

              Many benthic marine animal populations are established and maintained by free-swimming larvae that recognize cues from surface-bound bacteria to settle and metamorphose. Larvae of the tubeworm Hydroides elegans, an important biofouling agent, require contact with surface-bound bacteria to undergo metamorphosis; however, the mechanisms that underpin this microbially mediated developmental transition have been enigmatic. Here, we show that a marine bacterium, Pseudoalteromonas luteoviolacea, produces arrays of phage tail-like structures that trigger metamorphosis of H. elegans. These arrays comprise about 100 contractile structures with outward-facing baseplates, linked by tail fibers and a dynamic hexagonal net. Not only do these arrays suggest a novel form of bacterium-animal interaction, they provide an entry point to understanding how marine biofilms can trigger animal development.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                15 December 2016
                2016
                : 7
                : 1982
                Affiliations
                [1] 1Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine Chicago, IL, USA
                [2] 2Department of Microbiology and Plant Biology, University of Oklahoma Norman, OK, USA
                Author notes

                Edited by: Robert Brucker, Rowland Institute at Harvard, USA

                Reviewed by: Spencer V. Nyholm, University of Connecticut, USA; John M. Chaston, Brigham Young University, USA

                *Correspondence: Mark J. Mandel, m-mandel@ 123456northwestern.edu

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.01982
                5156696
                28018314
                cc5aabba-6bf2-4dfc-8c89-bdf474b26cbc
                Copyright © 2016 Mandel and Dunn.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 September 2016
                : 25 November 2016
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 85, Pages: 10, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: IOS-1456963, MCB-1050687
                Funded by: National Institute of General Medical Sciences 10.13039/100000057
                Award ID: R35GM119627
                Funded by: National Institute of Allergy and Infectious Diseases 10.13039/100000060
                Award ID: R21AI117262
                Categories
                Microbiology
                Review

                Microbiology & Virology
                symbiosis,microbiome,invertebrate model,marine microbiology,epithelial colonization,evolution

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