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      Borrelia burgdorferi Requires the Alternative Sigma Factor RpoS for Dissemination within the Vector during Tick-to-Mammal Transmission

      1 , 1 , 2 , 1 , 3 , 4 , 5 , *

      PLoS Pathogens

      Public Library of Science

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          Abstract

          While the roles of rpoS Bb and RpoS-dependent genes have been studied extensively within the mammal, the contribution of the RpoS regulon to the tick-phase of the Borrelia burgdorferi enzootic cycle has not been examined. Herein, we demonstrate that RpoS-dependent gene expression is prerequisite for the transmission of spirochetes by feeding nymphs. RpoS-deficient organisms are confined to the midgut lumen where they transform into an unusual morphotype (round bodies) during the later stages of the blood meal. We show that round body formation is rapidly reversible, and in vitro appears to be attributable, in part, to reduced levels of Coenzyme A disulfide reductase, which among other functions, provides NAD + for glycolysis. Our data suggest that spirochetes default to an RpoS-independent program for round body formation upon sensing that the energetics for transmission are unfavorable.

          Author Summary

          Lyme disease, caused by the spirochetal pathogen Borrelia burgdorferi, is the most prevalent arthropod-borne infection in the United States. In order to maintain itself in nature, B. burgdorferi must cycle between its arthropod vector, Ixodes ticks, and a mammalian reservoir, usually a small rodent. Previous studies have demonstrated that the alternative sigma factor RpoS is essential for B. burgdorferi to infect a mammalian host, whereas a role within the tick has never been examined. In this study, we determined that one or more RpoS-dependent genes are required for B. burgdorferi to disseminate through the tick. Using a combination of microscopy techniques, we show that RpoS-deficient organisms are confined to the lumen of the tick midgut during nymphal feeding where they form round bodies, while wild-type spirochetes remain elongated and traverse the midgut to enter the hemolymph and salivary glands en route to the mammalian host.

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          Most cited references 67

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          The RpoS-mediated general stress response in Escherichia coli.

          Under conditions of nutrient deprivation or stress, or as cells enter stationary phase, Escherichia coli and related bacteria increase the accumulation of RpoS, a specialized sigma factor. RpoS-dependent gene expression leads to general stress resistance of cells. During rapid growth, RpoS translation is inhibited and any RpoS protein that is synthesized is rapidly degraded. The complex transition from exponential growth to stationary phase has been partially dissected by analyzing the induction of RpoS after specific stress treatments. Different stress conditions lead to induction of specific sRNAs that stimulate RpoS translation or to induction of small-protein antiadaptors that stabilize the protein. Recent progress has led to a better, but still far from complete, understanding of how stresses lead to RpoS induction and what RpoS-dependent genes help the cell deal with the stress.
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            Multiple sigma subunits and the partitioning of bacterial transcription space.

            Promoter recognition in eubacteria is carried out by the initiation factor sigma, which binds RNA polymerase and initiates transcription. Cells have one housekeeping factor and a variable number of alternative sigma factors that possess different promoter-recognition properties. The cell can choose from its repertoire of sigmas to alter its transcriptional program in response to stress. Recent structural information illuminates the process of initiation and also shows that the two key sigma domains are structurally conserved, even among diverse family members. We use the sigma repertoire of Escherichia coli, Bacillus subtilis, Streptomyces coelicolor, and cyanobacteria to illustrate the different strategies utilized to organize transcriptional space using multiple sigma factors.
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              Induction of an outer surface protein on Borrelia burgdorferi during tick feeding.

              Lyme disease spirochetes, Borrelia burgdorferi sensu lato, are maintained in zoonotic cycles involving ticks and small mammals. In unfed ticks, the spirochetes produce one outer surface protein, OspA, but not OspC. During infection in mammals, immunological data suggest that the spirochetes have changed their surface, now expressing OspC but little or no OspA. We find by in vitro growth experiments that this change is regulated in part by temperature; OspC is produced by spirochetes at 32-37 degrees C but not at 24 degrees C. Furthermore, spirochetes in the midgut of ticks that have fully engorged on mice now have OspC on their surface. Thus two environmental cues, an increase in temperature and tick feeding, trigger a major alteration of the spirochetal outer membrane. This rapid synthesis of OspC by spirochetes during tick feeding may play an essential role in the capacity of these bacteria to successfully infect mammalian hosts, including humans, when transmitted by ticks.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                February 2012
                February 2012
                16 February 2012
                : 8
                : 2
                Affiliations
                [1 ]Department of Medicine, University of Connecticut Health Center, Farmington, Connecticut, United States of America
                [2 ]Department of Biomedical Sciences, Quinnipiac University, Hamden, Connecticut, United States of America
                [3 ]Department of Pediatrics, University of Connecticut Health Center, Farmington, Connecticut, United States of America
                [4 ]Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, Connecticut, United States of America
                [5 ]Department of Immunology, University of Connecticut Health Center, Farmington, Connecticut, United States of America
                Medical College of Wisconsin, United States of America
                Author notes

                Conceived and designed the experiments: SMDE MJC CHE JDR. Performed the experiments: SMDE MJC CHE. Analyzed the data: SMDE MJC CHE JDR. Contributed reagents/materials/analysis tools: SMDE MJC CHE JDR. Wrote the paper: SMDE MJC JDR.

                Article
                PPATHOGENS-D-11-02228
                10.1371/journal.ppat.1002532
                3280991
                22359504
                Dunham-Ems et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Genetics
                Gene Expression
                Microbiology
                Vector Biology

                Infectious disease & Microbiology

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