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      A Novel Bacterial Pathogen of Biomphalaria glabrata: A Potential Weapon for Schistosomiasis Control?

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          Abstract

          Background

          Schistosomiasis is the second-most widespread tropical parasitic disease after malaria. Various research strategies and treatment programs for achieving the objective of eradicating schistosomiasis within a decade have been recommended and supported by the World Health Organization. One of these approaches is based on the control of snail vectors in endemic areas. Previous field studies have shown that competitor or predator introduction can reduce snail numbers, but no systematic investigation has ever been conducted to identify snail microbial pathogens and evaluate their molluscicidal effects.

          Methodology/Principal findings

          In populations of Biomphalaria glabrata snails experiencing high mortalities, white nodules were visible on snail bodies. Infectious agents were isolated from such nodules. Only one type of bacteria, identified as a new species of Paenibacillus named Candidatus Paenibacillus glabratella, was found, and was shown to be closely related to P. alvei through 16S and Rpob DNA analysis. Histopathological examination showed extensive bacterial infiltration leading to overall tissue disorganization. Exposure of healthy snails to Paenibacillus-infected snails caused massive mortality. Moreover, eggs laid by infected snails were also infected, decreasing hatching but without apparent effects on spawning. Embryonic lethality was correlated with the presence of pathogenic bacteria in eggs.

          Conclusions/Significance

          This is the first account of a novel Paenibacillus strain, Ca. Paenibacillus glabratella, as a snail microbial pathogen. Since this strain affects both adult and embryonic stages and causes significant mortality, it may hold promise as a biocontrol agent to limit schistosomiasis transmission in the field.

          Author Summary

          The present paper reports the isolation and the characterization of a new microbial pathogen of the freshwater snail, Biomphalaria glabrata. Genetic analyses revealed that the species has not been previously described and could be classified into the Paenibacillus genus. These bacteria invade most snail tissues and proliferate, causing massive lethality. Moreover, the bacterial infection can be transmitted both vertically and horizontally to other snails, causing their death in 30 days. This discovery is potentially important because B. glabrata, as an intermediate host, plays an important role in transmitting schistosomiasis, the second-most widespread human parasitic disease. The World Health Organization’s objective of schistosomiasis eradication in a decade encourages the development of multiple approaches for countering the disease, one of which is vector population control. This new bacterial strain clearly could be a potential agent for such a strategy.

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          Most cited references78

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          The global status of schistosomiasis and its control.

          Schistosomiasis is being successfully controlled in many countries but remains a major public health problem, with an estimated 200 million people infected, mostly in Africa. Few countries in this region have undertaken successful and sustainable control programmes. The construction of water schemes to meet the power and agricultural requirements for development have lead to increasing transmission, especially of Schistosoma mansoni. Increasing population and movement have contributed to increased transmission and introduction of schistosomiasis to new areas. Most endemic countries are among the least developed whose health systems face difficulties to provide basic care at the primary health level. Constraints to control include, the lack of political commitment and infrastructure for public health interventions. Another constraint is that available anti-schistosomal drugs are expensive and the cost of individual treatment is a high proportion of the per capita drug budgets. There is need for increased support for schistosomiasis control in the most severely affected countries.
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            Bacillus thuringiensis: A story of a successful bioinsecticide.

            Bacillus thuringiensis (Bt) bacteria are insect pathogens that rely on insecticidal pore forming proteins known as Cry and Cyt toxins to kill their insect larval hosts. At least four different non-structurally related families of proteins form the Cry toxin group of toxins. The expression of certain Cry toxins in transgenic crops has contributed to an efficient control of insect pests resulting in a significant reduction in chemical insecticide use. The mode of action of the three domain Cry toxin family involves sequential interaction of these toxins with several insect midgut proteins facilitating the formation of a pre-pore oligomer structure and subsequent membrane insertion that leads to the killing of midgut insect cells by osmotic shock. In this manuscript we review recent progress in understanding the mode of action of this family of proteins in lepidopteran, dipteran and coleopteran insects. Interestingly, similar Cry-binding proteins have been identified in the three insect orders, as cadherin, aminopeptidase-N and alkaline phosphatase suggesting a conserved mode of action. Also, recent data on insect responses to Cry toxin attack is discussed. Finally, we review the different Bt based products, including transgenic crops, that are currently used in agriculture. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology.

              An ad hoc committee for the re-evaluation of the species definition in bacteriology met in Gent, Belgium, in February 2002. The committee made various recommendations regarding the species definition in the light of developments in methodologies available to systematists.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                26 February 2015
                February 2015
                : 9
                : 2
                : e0003489
                Affiliations
                [1 ]CNRS, UMR 5244, Ecologie et Evolution des Interactions (2EI), Perpignan, France
                [2 ]Université de Perpignan Via Domitia, Perpignan, France
                [3 ]Laboratoire de Chimie des Biomolécules et de l’Environnement (LCBE, EA 4215), Perpignan, France
                George Washington University School of Medicine and Health Sciences, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DD RG BG. Performed the experiments: DD RG JFA CC AR NA. Analyzed the data: DD RG BG ET GMo. Contributed reagents/materials/analysis tools: DD RG GMo ET JFA JP CC AR NA GMi AT BG. Wrote the paper: DD RG GMo GMi ET BG.

                Article
                PNTD-D-14-01688
                10.1371/journal.pntd.0003489
                4342248
                25719489
                b5b4d250-e13b-4b15-a567-c567da565ed3
                Copyright @ 2015

                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

                History
                : 29 September 2014
                : 17 December 2014
                Page count
                Figures: 8, Tables: 0, Pages: 20
                Funding
                This work was supported by funds from the Centre National de la Recherche (CNRS) and the Universite de Perpignan Via Domitia (UPVD), and by a grant from the ANR JCJC INVIMORY number ANR-13-JSV7-0009. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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