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      Modifying and reacting to the environmental pH can drive bacterial interactions

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      PLoS Biology
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          Abstract

          Microbes usually exist in communities consisting of myriad different but interacting species. These interactions are typically mediated through environmental modifications; microbes change the environment by taking up resources and excreting metabolites, which affects the growth of both themselves and also other microbes. We show here that the way microbes modify their environment and react to it sets the interactions within single-species populations and also between different species. A very common environmental modification is a change of the environmental pH. We find experimentally that these pH changes create feedback loops that can determine the fate of bacterial populations; they can either facilitate or inhibit growth, and in extreme cases will cause extinction of the bacterial population. Understanding how single species change the pH and react to these changes allowed us to estimate their pairwise interaction outcomes. Those interactions lead to a set of generic interaction motifs—bistability, successive growth, extended suicide, and stabilization—that may be independent of which environmental parameter is modified and thus may reoccur in different microbial systems.

          Author summary

          Microbes typically live alongside many other species in complex communities. These microbial communities are very important for us because they also live in and on our bodies and can determine our health and well-being. The composition and function of these communities, such as who is part of such a community and who is excluded, are decided by the interactions between the microbes. These microbial interactions can be driven by many different factors such as resource competition or toxin production. Although these factors are all different, the interactions are typically mediated through the environment; the microbes modify the environment, and they and other microbes have to live in this new environment. We show here that by understanding how microbes change and react to the environment, it is possible to understand and even predict their interactions. We believe that this way of thinking about microbial interactions will lead to a better understanding of more complex communities that are so important for our well-being.

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          Most cited references38

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          The diversity and biogeography of soil bacterial communities.

          For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
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            Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization.

            The influence of pH on the relative importance of the two principal decomposer groups in soil, fungi and bacteria, was investigated along a continuous soil pH gradient at Hoosfield acid strip at Rothamsted Research in the United Kingdom. This experimental location provides a uniform pH gradient, ranging from pH 8.3 to 4.0, within 180 m in a silty loam soil on which barley has been continuously grown for more than 100 years. We estimated the importance of fungi and bacteria directly by measuring acetate incorporation into ergosterol to measure fungal growth and leucine and thymidine incorporation to measure bacterial growth. The growth-based measurements revealed a fivefold decrease in bacterial growth and a fivefold increase in fungal growth with lower pH. This resulted in an approximately 30-fold increase in fungal importance, as indicated by the fungal growth/bacterial growth ratio, from pH 8.3 to pH 4.5. In contrast, corresponding effects on biomass markers for fungi (ergosterol and phospholipid fatty acid [PLFA] 18:2omega6,9) and bacteria (bacterial PLFAs) showed only a two- to threefold difference in fungal importance in the same pH interval. The shift in fungal and bacterial importance along the pH gradient decreased the total carbon mineralization, measured as basal respiration, by only about one-third, possibly suggesting functional redundancy. Below pH 4.5 there was universal inhibition of all microbial variables, probably derived from increased inhibitory effects due to release of free aluminum or decreasing plant productivity. To investigate decomposer group importance, growth measurements provided significantly increased sensitivity compared with biomass-based measurements.
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              Bacteriocins: evolution, ecology, and application.

              Microbes produce an extraordinary array of microbial defense systems. These include classical antibiotics, metabolic by-products, lytic agents, numerous types of protein exotoxins, and bacteriocins. The abundance and diversity of this potent arsenal of weapons are clear. Less clear are their evolutionary origins and the role they play in mediating microbial interactions. The goal of this review is to explore what we know about the evolution and ecology of the most abundant and diverse family of microbial defense systems: the bacteriocins. We summarize current knowledge of how such extraordinary protein diversity arose and is maintained in microbial populations and what role these toxins play in mediating microbial population-level and community-level dynamics. In the latter half of this review we focus on the potential role bacteriocins may play in addressing human health concerns and the current role they serve in food preservation.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                14 March 2018
                March 2018
                14 March 2018
                : 16
                : 3
                : e2004248
                Affiliations
                [001]Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
                Synthetic and Systems Biology Unit, Hungary
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-4583-8555
                Article
                pbio.2004248
                10.1371/journal.pbio.2004248
                5868856
                29538378
                02cc5f7a-761c-468e-b457-e3f20c50a498

                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
                : 14 September 2017
                : 14 February 2018
                Page count
                Figures: 4, Tables: 0, Pages: 20
                Funding
                Simons Foundation https://www.simonsfoundation.org/ (grant number 6936338). Received by JG. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NIH https://www.nih.gov/ (grant number 6936234). Received by JG. The funder 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
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Serratia Marcescens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Serratia Marcescens
                Biology and Life Sciences
                Organisms
                Bacteria
                Enterobacteriaceae
                Serratia
                Serratia Marcescens
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Urea
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Urea
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Carbohydrates
                Monosaccharides
                Glucose
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Carbohydrates
                Monosaccharides
                Glucose
                Biology and Life Sciences
                Organisms
                Bacteria
                Physical Sciences
                Physics
                Nuclear Physics
                Nucleons
                Protons
                Biology and Life Sciences
                Species Interactions
                Physical Sciences
                Chemistry
                Chemical Compounds
                Phosphates
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-03-26
                All relevant data are within the paper and its Supporting Information files.

                Life sciences
                Life sciences

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