Taxonomic and functional shifts in the beech rhizosphere microbiome across a natural soil toposequence

www.nature.com/scientificreports OPEN Received: 23 February 2017 Accepted: 13 July 2017 Published: xx xx xxxx Taxonomic and functional shifts in the beech rhizosphere microbiome across a natural soil toposequence Y. Colin1,2, O. Nicolitch 1,2 , J. D. Van Nostrand 3 , J. Z. Zhou3,4,5, M.-P. Turpault1,2 & S. Uroz1,2 It has been rarely questioned as to whether the enrichment of specific bacterial taxa found in the rhizosphere of a given plant species changes with different soil types under field conditions and under similar climatic conditions. Understanding tree microbiome interactions is essential because, in contrast to annual plants, tree species require decades to grow and strongly depend on the nutritive resources of the soil. In this context, we tested using a natural toposequence the hypothesis that beech trees select specific taxa and functions in their rhizosphere based on the soil conditions and their nutritive requirements. Our 16S rRNA gene pyrosequencing analyses revealed that the soil type determines the taxa colonizing the beech rhizosphere. A rhizosphere effect was observed in each soil type, but a stronger effect was observed in the nutrient-poor soils. Although the communities varied significantly across the toposequence, we identified a core beech rhizosphere microbiome. Functionally, GeoChip analyses showed a functional redundancy across the toposequence, with genes related to nutrient cycling and to the bacterial immune system being significantly enriched in the rhizosphere. Altogether, the data suggest that, regardless of the soil conditions, trees enrich variable bacterial communities to maintain the functions necessary for their nutrition. Plants are known for their ability to colonize a wide range of terrestrial environments and to adapt to various climatic or edaphic constraints1. As an example, the distribution of deciduous and coniferous trees in forest ecosystems is determined by local environmental factors such as climate, water availability and soil type2, 3. In boreal regions, forests are dominated by coniferous tree species adapted to low temperatures, such as Picea abies. In contrast, temperate regions are dominated by Fagus sylvatica L., which presents a broader area of distribution despite having a high sensitivity to drought and high temperatures4–6. The broad distribution of beech in soils developed on calcareous to acidic mineral parental materials is currently explained by its high tolerance to various soil parameters such as pH, nutrients availability, water content compared to other tree species6. Notably, several studies have highlighted that beech trees harbour variable densities of fine root biomass (roots devoted to nutrient access) in the topsoil depending on the soil acidity and/or nutrient availability6–8. Such adaptation of beech trees to acidic conditions, which are characterized by low nutrient availability, suggests a strong investment by this tree species in soil exploration and nutrient access. The adaptation of beech trees to low nutrient soils may be partly due to its ability to produce root exudates and to select within its root vicinity microorganisms capable of accessing nutrients9. Indeed, plants are known to produce a wide range of compounds, including protons, organic acids, amino acids, carbohydrates, phytosiderophores and signal molecules10–12. Through these compounds, the production of which is regulated by plant age, root maturity and nutrient availability, plants modify the soil physico-chemical characteristics to fit their nutritional requirements10, 13–16. In this sense, Augusto et al.17 revealed that trees impact soil chemistry, showing that coniferous trees strongly increase nutrient availability compared to deciduous species such as beech or oak through the acidification of the soil. Comparisons of the bulk soil and rhizosphere compartments below beech, Douglas fir or Norway spruce revealed an increase in the nutrient availability in the rhizosphere compared to 1 INRA, Université de Lorraine, UMR 1136 “Interactions Arbres Micro-organismes”, Centre INRA de Nancy, 54280, Champenoux, France. 2INRA UR 1138 “Biogéochimie des Ecosystèmes Forestiers”, Centre INRA de Nancy, 54280, Champenoux, France. 3Institute for Environmental Genomics, and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73072, USA. 4Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA. 5State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China. Correspondence and requests for materials should be addressed to S.U. (email: ) Scientific ReporTS | 7: 9604 | DOI:10.1038/s41598-017-07639-1 1 www.nature.com/scientificreports/ the bulk soil, suggesting that active processes occur in the rhizosphere to access nutritive elements entrapped in organic matter and soil minerals18, 19. In addition to acidification process, the rhizosphere provides a carbon-rich environment that is favourable to bacterial communities11, 16, 20–25. Indeed, the enrichment of specific bacterial communities in the rhizosphere has been well-established for a wide range of perennial and non-perennial plants26–33. Notably, the enriched communities in the rhizosphere harbour functional traits capable of improving nutrient cycling, plant nutrition or protection against pathogens, suggesting plants select effective bacterial partners in their rhizosphere34, 35. Such selection has been evidenced in acidic and nutrient-poor forest soils, showing the enrichment of effective mineral-weathering bacteria in the rhizosphere of various tree species, including beech, oak and Norway spruce9, 36, 37. This selective process was also reported for non-perennial plants and in other ecosystems38–41. These studies highlighted that the bacterial communities occurring in the soil reservoir vary based on the soil type and its physico-chemical properties, and especially the pH38, 39, 41–44. However, it remains extremely difficult to disentangle whether the observed effect is directly related to pH or indirectly affected by variation in other co-varying edaphic parameters41. Indeed, soil pH modulates other edaphic parameters such as nutrient availability, aluminium availability, organic carbon and phosphorus45, which may in turn influence soil bacterial communities. Altogether, these studies clearly demonstrate that soil edaphic parameters and the tree rhizosphere each strongly determine the diversity, structure and functioning of soil bacterial communities33, 43. However, the extent to which both associated factors contribute to shaping forest soil microbiomes is not fully understood and is likely to vary depending on the edaphic conditions and tree physiology. Understanding tree microbiome interactions is essential as, in contrast to annual plants, trees need decades to grow and strongly depend on the nutritive resources in the soil. (...truncated)