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      Interactions between Bacillus anthracis and Plants May Promote Anthrax Transmission

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          Abstract

          Environmental reservoirs are essential in the maintenance and transmission of anthrax but are poorly characterized. The anthrax agent, Bacillus anthracis was long considered an obligate pathogen that is dormant and passively transmitted in the environment. However, a growing number of laboratory studies indicate that, like some of its close relatives, B. anthracis has some activity outside of its vertebrate hosts. Here we show in the field that B. anthracis has significant interactions with a grass that could promote anthrax spore transmission to grazing hosts. Using a local, virulent strain of B. anthracis, we performed a field experiment in an enclosure within a grassland savanna. We found that B. anthracis increased the rate of establishment of a native grass ( Enneapogon desvauxii) by 50% and that grass seeds exposed to blood reached heights that were 45% taller than controls. Further we detected significant effects of E. desvauxii, B. anthracis, and their interaction on soil bacterial taxa richness and community composition. We did not find any evidence for multiplication or increased longevity of B. anthracis in bulk soil associated with grass compared to controls. Instead interactions between B. anthracis and plants may result in increased host grazing and subsequently increased transmission to hosts.

          Author Summary

          Anthrax is a neglected zoonotic disease affecting livestock, wildlife, and humans in developing countries, particularly in Africa and Asia, and it occurs regularly in rural parts of North America. The causative agent of anthrax, Bacillus anthracis is transmitted by spores that persist for long periods of time in the environment. The transmission mechanisms of socioeconomically important and environmentally maintained pathogens are poorly understood, yet essential for understanding disease dynamics and devising appropriate control measures. Recent laboratory studies show that B. anthracis interacts with plants and other soil-dwelling organisms that may affect its survival and transmission. In this paper, we describe the results of a field experiment designed to test whether the interaction of B. anthracis with plants might affect its persistence and potential transmission to grazing hosts. We found that like some of its close relatives, B. anthracis promotes plant growth. Rather than simply lying in wait as a dormant spore in soil, instead B. anthracis may promote plant growth as a way of attracting hosts to graze on infectious material at carcass sites.

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          Most cited references35

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          Microbial co-operation in the rhizosphere.

          Soil microbial populations are immersed in a framework of interactions known to affect plant fitness and soil quality. They are involved in fundamental activities that ensure the stability and productivity of both agricultural systems and natural ecosystems. Strategic and applied research has demonstrated that certain co-operative microbial activities can be exploited, as a low-input biotechnology, to help sustainable, environmentally-friendly, agro-technological practices. Much research is addressed at improving understanding of the diversity, dynamics, and significance of rhizosphere microbial populations and their co-operative activities. An analysis of the co-operative microbial activities known to affect plant development is the general aim of this review. In particular, this article summarizes and discusses significant aspects of this general topic, including (i) the analysis of the key activities carried out by the diverse trophic and functional groups of micro-organisms involved in co-operative rhizosphere interactions; (ii) a critical discussion of the direct microbe-microbe interactions which results in processes benefiting sustainable agro-ecosystem development; and (iii) beneficial microbial interactions involving arbuscular mycorrhiza, the omnipresent fungus-plant beneficial symbiosis. The trends of this thematic area will be outlined, from molecular biology and ecophysiological issues to the biotechnological developments for integrated management, to indicate where research is needed in the future.
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            Applications of free living plant growth-promoting rhizobacteria.

            Free-living plant growth-promoting rhizobacteria (PGPR) can be used in a variety of ways when plant growth enhancements are required. The most intensively researched use of PGPR has been in agriculture and horticulture. Several PGPR formulations are currently available as commercial products for agricultural production. Recently developing areas of PGPR usage include forest regeneration and phytoremediation of contaminated soils. As the mechanisms of plant growth promotion by these bacteria are unravelled, the possibility of more efficient plant-bacteria pairings for novel and practical uses will follow. The progress to date in using PGPR in a variety of applications with different plants is summarized and discussed here.
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              Interactions of Bacillus spp. and plants--with special reference to induced systemic resistance (ISR).

              Biological control of soil-borne pathogens comprises the decrease of inoculum or of the disease producing activity of a pathogen through one or more mechanisms. Interest in biological control of soil-borne plant pathogens has increased considerably in the last few decades, because it may provide control of diseases that cannot or only partly be managed by other control strategies. Recent advances in microbial and molecular techniques have significantly contributed to new insights in underlying mechanisms by which introduced bacteria function. Colonization of plant roots is an essential step for both soil-borne pathogenic and beneficial rhizobacteria. Colonization patterns showed that rhizobacteria act as biocontrol agents or as growth-promoting bacteria form microcolonies or biofilms at preferred sites of root exudation. Such microcolonies are sites for bacteria to communicate with each other (quorum sensing) and to act in a coordinated manner. Elicitation of induced systemic resistance (ISR) by plant-associated bacteria was initially demonstrated using Pseudomonas spp. and other Gram-negative bacteria. Several strains of the species Bacillus amyloliquefaciens, B. subtilis, B. pasteurii, B. cereus, B. pumilus, B. mycoides, and B. sphaericus elicit significant reductions in the incidence or severity of various diseases on a diversity of hosts. Elicitation of ISR by these strains has been demonstrated in greenhouse or field trials on tomato, bell pepper, muskmelon, watermelon, sugar beet, tobacco, Arabidopsis sp., cucumber, loblolly pine, and two tropical crops (long cayenne pepper and green kuang futsoi). Protection resulting from ISR elicited by Bacillus spp. has been reported against leaf-spotting fungal and bacterial pathogens, systemic viruses, a crown-rotting fungal pathogen, root-knot nematodes, and a stem-blight fungal pathogen as well as damping-off, blue mold, and late blight diseases. This progress will lead to a more efficient use of these strains which is worthwhile approach to explore in context of biocontrol strategies.
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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, USA )
                1935-2727
                1935-2735
                June 2014
                5 June 2014
                : 8
                : 6
                : e2903
                Affiliations
                [1 ]Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, California, United States of America
                [2 ]Ecology Department, Earth Science Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America
                [3 ]Independent researcher, Windhoek, Namibia
                [4 ]Department of Statistics, University of California, Berkeley, California, United States of America
                [5 ]Ministry of Fisheries and Marine Resources, Inland Aquaculture, Katima Mulilo Regional Office, Katima Mulilo, Namibia
                [6 ]School of Mathematical Sciences, University of KwaZulu-Natal, Durban, South Africa
                University of California San Diego School of Medicine, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HHG WCT ELB TT WMG. Performed the experiments: HHG MK HS. Analyzed the data: HHG ELB YS. Contributed reagents/materials/analysis tools: HHG WCT ELB TT WMG. Wrote the paper: HHG WCT ELB MK YS HS TT WMG.

                [¤a]

                Current address: Genome Center and Department of Evolution and Ecology, University of California, Davis, Davis, California, United States of America

                [¤b]

                Current address: Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Oslo, Norway

                Article
                PNTD-D-13-01944
                10.1371/journal.pntd.0002903
                4046938
                24901846
                96917266-add2-4f8f-a551-3c6a1b68cca0
                Copyright @ 2014

                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.

                History
                : 6 December 2013
                : 14 April 2014
                Page count
                Pages: 11
                Funding
                This project was funded by NIH Grant GM083863 to WMG. The PhyloChip laboratory work was performed at Lawrence Berkeley National Laboratory under contract number DE-AC02-05CH11231 with the Department of Energy, Office of Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Microbial Ecology
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Veterinary Science
                Veterinary Diseases
                Zoonoses
                Anthrax
                Veterinary Bacteriology
                Veterinary Microbiology
                Ecology and Environmental Sciences
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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