Abstract
BackgroundSoils are a key component of agricultural productivity, and soil microbiota determine the availability of many essential plant nutrients. Agricultural domestication of soils, that is, the conversion of previously uncultivated soils to a cultivated state, is frequently accompanied by intensive monoculture, especially in the developing world. However, there is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domestication, including to what extent crop plants impact soil microbiota composition, and how changes in microbiota composition arising from cultivation affect crop performance.ResultsWe show here that continuous monoculture (> 8 growing seasons) of the major food crop rice under flooded conditions is associated with a pronounced shift in soil bacterial and archaeal microbiota structure towards a more consistent composition, thereby domesticating microbiota of previously uncultivated sites. Aside from the potential effects of agricultural cultivation practices, we provide evidence that rice plants themselves are important drivers of the domestication process, acting through selective enrichment of specific taxa, including methanogenic archaea, in their rhizosphere that differ from those of native plants growing in the same environment. Furthermore, we find that microbiota from soils domesticated by rice cultivation contribute to plant-soil feedback, by imparting a negative effect on rice seedling vigor.ConclusionsSoil domestication through continuous monoculture cultivation of rice results in compositional changes in the soil microbiota, which are in part driven by the rice plants. The consequences include a negative impact on plant performance and increases in greenhouse gas emitting microbes.
Highlights
Plant roots are colonized by complex microbiota that are largely derived from the surrounding soil [1,2,3,4]
We investigated the following three questions: (1) Does long-term rice cultivation change the bacterial and archaeal components of the soil microbiome? (2) Is the rice plant itself a driver of the soil domestication process at the microbial level? (3) What is the impact on host plant vigor of domesticated microbiomes compared to microbiomes of undomesticated soils? The results provide insights into the impacts of continuous cultivation of rice on bacterial and archaeal soil microbiota and the consequences of soil domestication through agriculture on rice plant vigor
Soil cultivation history impacts plant root microbial assemblages To evaluate the effect of intensive rice cultivation on the bacterial and archaeal diversity inhabiting the soil-root continuum, we surveyed the prokaryotic taxonomic composition of bulk soil, rhizosphere, and endosphere communities of rice plants grown in cultivated and noncultivated soils under flooded conditions in a greenhouse
Summary
Plant roots are colonized by complex microbiota that are largely derived from the surrounding soil [1,2,3,4]. Cultivation of maize has been recently reported to restructure soil microbial diversity in prairie soils; the observed changes were attributed to agricultural practices rather than driven by maize plants [21]. Arising from these and earlier studies are unresolved but important questions, as to whether detrimental effects originating from altered microbiota are a general feature of intensive agriculture, and to what extent the crop plant itself, as opposed to agricultural practices, drives such changes in the microbiome. There is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domestication, including to what extent crop plants impact soil microbiota composition, and how changes in microbiota composition arising from cultivation affect crop performance
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