Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota

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.

Diversity, function and assembly of mangrove root-associated microbial communities at a continuous fine-scale

“…However, the effect of root exudates on rhizobiome assembly is complicated, and the strategy of rootassociated microbial community assembly at the soil-root interface remains controversial. The findings of some studies on root-associated microbiota in rice corroborate a two-step or multiple-step model in the root microbiota assembly, where specific microbial taxa in soil gradually become depleted or enriched during root colonization 15,22 . Other studies on rice and Medicago root-associated microbiota pointed to the applicability of the amplification-selection process, where dominant phyla would undergo substantial enrichment in the rhizosphere followed by the specific recruitment of certain phyla into the roots 23 .…”

Microbial Diversity of Upland Rice Roots and Their Influence on Rice Growth and Drought Tolerance

“…Rice ( Oryza sativa L.) exists as two ecotypes, upland and irrigated ecotypes, which are adapted to rainfed upland conditions and well-watered conditions, respectively [ 40 , 41 ]. However, previous studies on the rice microbiome or PGPR have focused mainly on irrigated rice [ 11 , 42 , 43 , 44 , 45 , 46 , 47 , 48 ]. Recent studies have proven that there may be great differences between root microbes of irrigated rice and drought-stressed rice [ 10 , 49 , 50 ].…”

Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters

“…Furthermore, a study has recently shown that Methanobacterium OTUs were more enriched in the endosphere of rice plants than in other native plant species growing in the same field, indicating that Methanobacterium spp. have a unique interaction with rice (45). Previous studies have correlated the activity of superoxide dismutase with oxygen tolerance in some taxa, including Methanobacterium, as well as some anaerobic taxa discussed above (e.g., Desulfovibrio and Propionivibrio) (46)(47)(48).…”