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      The Legionella pneumophila GIG operon responds to gold and copper in planktonic and biofilm cultures

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          Abstract

          Legionella pneumophila contaminates man-made water systems and creates numerous exposure risks for Legionnaires’ Disease. Because copper/silver ionization is commonly used to control L. pneumophila, its mechanisms of metal response and detoxification are of significant interest. Here we describe an L. pneumophila operon with significant similarity to the GIG operon of Cupriavidus metallidurans. The Legionella GIG operon is present in a subset of strains and has been acquired as part of the ICE-βox 65-kB integrative conjugative element. We assessed GIG promoter activity following exposure of L. pneumophila to multiple concentrations of HAuCl 4, CuSO 4 and AgNO 3. At 37°C, control stationary phase cultures exhibited GIG promoter activity. This activity increased significantly in response to 20 and 50uM HAuCl 4 and CuSO 4 but not in response to AgNO 3. Conversely, at 26°C, cultures exhibited decreased promoter response to copper. GIG promoter activity was also induced by HAuCl 4 or CuSO 4 during early biofilm establishment at both temperatures. When an L. pneumophila GIG promoter construct was transformed into E. coli DH5α, cultures showed baseline expression levels that did not increase following metal addition. Analysis of L. pneumophila transcriptional regulatory mutants suggested that GIG up-regulation in the presence of metal ions may be influenced by the stationary phase sigma factor, RpoS.

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          Most cited references 52

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          Quantification of biofilm structures by the novel computer program COMSTAT.

          The structural organization of four microbial communities was analysed by a novel computer program, COMSTAT, which comprises ten features for quantifying three-dimensional biofilm image stacks. Monospecies biofilms of each of the four bacteria, Pseudomonas: putida, P. aureofaciens, P. fluorescens and P. aeruginosa, tagged with the green fluorescent protein (GFP) were grown in flow chambers with a defined minimal medium as substrate. Analysis by the COMSTAT program of four variables describing biofilm structure - mean thickness, roughness, substratum coverage and surface to volume ratio - showed that the four Pseudomonas: strains represent different modes of biofilm growth. P. putida had a unique developmental pattern starting with single cells on the substratum growing into micro-colonies, which were eventually succeeded by long filaments and elongated cell clusters. P. aeruginosa colonized the entire substratum, and formed flat, uniform biofilms. P. aureofaciens resembled P. aeruginosa, but had a stronger tendency to form micro-colonies. Finally, the biofilm structures of P. fluorescens had a phenotype intermediate between those of P. putida and P. aureofaciens. Analysis of biofilms of P. aureofaciens growing on 0.03 mM, 0.1 mM or 0.5 mM citrate minimal media showed that mean biofilm thickness increased with increasing citrate concentration. Moreover, biofilm roughness increased with lower citrate concentrations, whereas surface to volume ratio increased with higher citrate concentrations.
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            Microbial heavy-metal resistance.

            We are just beginning to understand the metabolism of heavy metals and to use their metabolic functions in biotechnology, although heavy metals comprise the major part of the elements in the periodic table. Because they can form complex compounds, some heavy metal ions are essential trace elements, but, essential or not, most heavy metals are toxic at higher concentrations. This review describes the workings of known metal-resistance systems in microorganisms. After an account of the basic principles of homoeostasis for all heavy-metal ions, the transport of the 17 most important (heavy metal) elements is compared.
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              Legionella and Legionnaires' disease: 25 years of investigation.

              There is still a low level of clinical awareness regarding Legionnaires' disease 25 years after it was first detected. The causative agents, legionellae, are freshwater bacteria with a fascinating ecology. These bacteria are intracellular pathogens of freshwater protozoa and utilize a similar mechanism to infect human phagocytic cells. There have been major advances in delineating the pathogenesis of legionellae through the identification of genes which allow the organism to bypass the endocytic pathways of both protozoan and human cells. Other bacteria that may share this novel infectious process are Coxiella burnetti and Brucella spp. More than 40 species and numerous serogroups of legionellae have been identified. Most diagnostic tests are directed at the species that causes most of the reported human cases of legionellosis, L. pneumophila serogroup 1. For this reason, information on the incidence of human respiratory disease attributable to other species and serogroups of legionellae is lacking. Improvements in diagnostic tests such as the urine antigen assay have inadvertently caused a decrease in the use of culture to detect infection, resulting in incomplete surveillance for legionellosis. Large, focal outbreaks of Legionnaires' disease continue to occur worldwide, and there is a critical need for surveillance for travel-related legionellosis in the United States. There is optimism that newly developed guidelines and water treatment practices can greatly reduce the incidence of this preventable illness.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2 May 2017
                2017
                : 12
                : 5
                Affiliations
                [1 ]Department of Biological Sciences, Clemson University, Clemson, South Carolina, United States of America
                [2 ]Clemson Light Imaging Facility, Clemson University, Clemson, South Carolina, United States of America
                Purdue University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: CW T. Bruce TM.

                • Data curation: CW T. Banks TM.

                • Formal analysis: KJ CW TM.

                • Funding acquisition: TM.

                • Investigation: KJ CW T. Banks JR T. Bruce.

                • Methodology: T. Bruce TM.

                • Project administration: TM.

                • Resources: CW T. Bruce TM.

                • Supervision: T. Bruce TM.

                • Validation: KJ TM.

                • Visualization: CW TM.

                • Writing – original draft: KJ CW JR T. Bruce TM.

                • Writing – review & editing: KJ CW T. Bruce JR T. Banks TM.

                Article
                PONE-D-16-16574
                10.1371/journal.pone.0174245
                5413113
                28463986

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Counts
                Figures: 8, Tables: 2, Pages: 17
                Product
                Funding
                Funded by: Clemson University (US)
                Award ID: Creative Inquiry Program
                Award Recipient :
                Clemson University Creative Inquiry Program provided funding through JR and TB participation in the project.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Bacteria
                Legionella
                Legionella Pneumophila
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Legionella
                Legionella Pneumophila
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Legionella
                Legionella Pneumophila
                Biology and Life Sciences
                Genetics
                DNA
                Operons
                Biology and Life Sciences
                Biochemistry
                Nucleic Acids
                DNA
                Operons
                Biology and Life Sciences
                Microbiology
                Bacteriology
                Bacterial Biofilms
                Biology and Life Sciences
                Microbiology
                Biofilms
                Bacterial Biofilms
                Biology and Life Sciences
                Organisms
                Bacteria
                Legionella
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Legionella
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Legionella
                Biology and Life Sciences
                Microbiology
                Biofilms
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Membrane Proteins
                Integral Membrane Proteins
                Biology and life sciences
                Biochemistry
                Proteins
                DNA-binding proteins
                Physical Sciences
                Chemistry
                Chemical Elements
                Gold
                Custom metadata
                All relevant data are within the paper.

                Uncategorized

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