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.

Highlights

  • Soil organic nutrient amendments are recognized for their potential to improve soil physicochemical properties and biological characteristics in agroecosystems, including carbon sequestration and nutrient availability, as well as microbial activity and biomass in the soil (Schutter and Dick, 2001; Gomez et al, 2006; Schlatter et al, 2009; Shi et al, 2011; Intanon et al, 2015; Regni et al, 2016)

  • Soil amendment with fructose resulted in the greatest difference in nutrient use profiles of Streptomyces isolates compared to the non-amended control

  • We hypothesized that the addition of carbon compounds to soil would impose selection that would result in shifts in nutrient use profiles, and antibiotic inhibitory and resistance phenotypes, of Streptomyces populations in agricultural soils

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Summary

Introduction

Soil organic nutrient amendments are recognized for their potential to improve soil physicochemical properties and biological characteristics in agroecosystems, including carbon sequestration and nutrient availability, as well as microbial activity and biomass in the soil (Schutter and Dick, 2001; Gomez et al, 2006; Schlatter et al, 2009; Shi et al, 2011; Intanon et al, 2015; Regni et al, 2016). Streptomyces are known for their antagonistic capacities and ability to suppress diverse plant pathogens (Samac and Kinkel, 2001; Xiao et al, 2002; Otto-Hanson et al, 2013; Law et al, 2017). Previous work suggests that competition for nutrients among coexisting Streptomyces mediates selection for antibiotic inhibitory capacity of soil Streptomyces (Kinkel et al, 2014). Streptomyces vary significantly in their ability to metabolize particular nutrients (Schlatter et al, 2013) and exhibit high specificity in antibiotic resistant and inhibitory interactions (Davelos et al, 2004), suggesting the potential for diverse resource and antagonistic competitive interactions among soil Streptomyces

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