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      Carbon Amendments Induce Shifts in Nutrient Use, Inhibitory, and Resistance Phenotypes Among Soilborne Streptomyces

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          Abstract

          Carbon amendments are used in agriculture for increasing microbial activity and biomass in the soil. Changes in microbial community composition and function in response to carbon additions to soil have been associated with biological suppression of soilborne diseases. However, the specific selective impacts of carbon amendments on microbial antagonistic populations are not well understood. We investigated the effects of soil carbon amendments on nutrient use profiles, and antibiotic inhibitory and resistance phenotypes of Streptomyces populations from agricultural soils. Soil mesocosms were amended at intervals over 9 months with low or high dose solutions of glucose, fructose, a complex amendment, or water only (non-amendment control). Over 130 Streptomyces isolates were collected from amended and non-amended mesocosm soils, and nutrient utilization profiles on 95 different carbon substrates were determined. A subset of isolates ( n = 40) was characterized for their ability to inhibit or resist one another. Carbon amendments resulted in Streptomyces populations with greater niche widths, and increased growth efficiencies as compared with Streptomyces in non-amended soils. Shifts in microbial nutrient use and growth capacities coincided with positive selection for Streptomyces antibiotic inhibitory phenotypes in carbon-amended soils, resulting in populations dominated by phenotypes that combine both antagonistic capacities and a generalist lifestyle. Carbon inputs resulted in populations that on average were more resistant to one another than populations in non-amended soils. Shifts in metabolic capacities and antagonistic activity indicate that carbon additions to soil may selectively enrich Streptomyces antagonistic phenotypes, that are rare under non-nutrient selection, but can inhibit more intensively nutrient competitors, and resist phenotypes with similar functional traits. These results shed light on the potential for using carbon amendments to strategically mediate soil microbial community assembly, and contribute to the establishment of pathogen-suppressive soils in agricultural systems.

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          Sampling the antibiotic resistome.

          Microbial resistance to antibiotics currently spans all known classes of natural and synthetic compounds. It has not only hindered our treatment of infections but also dramatically reshaped drug discovery, yet its origins have not been systematically studied. Soil-dwelling bacteria produce and encounter a myriad of antibiotics, evolving corresponding sensing and evading strategies. They are a reservoir of resistance determinants that can be mobilized into the microbial community. Study of this reservoir could provide an early warning system for future clinically relevant antibiotic resistance mechanisms.
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            Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls

            Soil organic matter (SOM) and the carbon and nutrients therein drive fundamental submicron- to global-scale biogeochemical processes and influence carbon-climate feedbacks. Consensus is emerging that microbial materials are an important constituent of stable SOM, and new conceptual and quantitative SOM models are rapidly incorporating this view. However, direct evidence demonstrating that microbial residues account for the chemistry, stability and abundance of SOM is still lacking. Further, emerging models emphasize the stabilization of microbial-derived SOM by abiotic mechanisms, while the effects of microbial physiology on microbial residue production remain unclear. Here we provide the first direct evidence that soil microbes produce chemically diverse, stable SOM. We show that SOM accumulation is driven by distinct microbial communities more so than clay mineralogy, where microbial-derived SOM accumulation is greatest in soils with higher fungal abundances and more efficient microbial biomass production.
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              Interference competition and niche theory.

              A linear model of interspecific competition with separate parameters for exploitation and interference is deduced. Interference is assumed to have a cost and an effect. The interfering species realizes a "profit" if some resources, which the species interfered against would have utilized, are made available as a result of the interference. Interference is favored when its cost is small, its effect is high, and the resource overlap with the species interfered against is high. Interference is likely to be an alternative strategy to high exploitation efficiency. The incorporation of interference into niche theory clarifies the competitive phenomenon of unstable equilibrium points, excess density compensation on islands, competitive avoidance by escape in time and space, the persistence of the "prudent predator," and the magnitude of the difference between the size of a species' fundamental niche and its realized niche.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                27 March 2019
                2019
                : 10
                : 498
                Affiliations
                Department of Plant Pathology, University of Minnesota , St. Paul, MN, United States
                Author notes

                Edited by: Marja Tiirola, University of Jyväskylä, Finland

                Reviewed by: Holly M. Simon, Oregon Health & Science University, United States; Suvi Suurnäkki, University of Jyväskylä, Finland

                *Correspondence: José Pablo Dundore-Arias, jdundore@ 123456umn.edu

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00498
                6445949
                30972036
                be21a43a-cbc0-4753-9cb4-0f03a6e87802
                Copyright © 2019 Dundore-Arias, Felice, Dill-Macky and Kinkel.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 August 2018
                : 26 February 2019
                Page count
                Figures: 5, Tables: 1, Equations: 1, References: 42, Pages: 11, Words: 0
                Funding
                Funded by: National Institute of Food and Agriculture 10.13039/100005825
                Award ID: 2011-67019-30200
                Funded by: National Science Foundation 10.13039/100000001
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                streptomyces,carbon amendments,soil mesocosms,resource use,antibiotic inhibition,antibiotic resistance

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