Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly

Liu et al. BMC Microbiology (2019) 19:201 https://doi.org/10.1186/s12866-019-1572-x RESEARCH ARTICLE Open Access Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly Fang Liu1, Tarek Hewezi2, Sarah L. Lebeis3, Vince Pantalone4, Parwinder S. Grewal5 and Margaret E. Staton6* Abstract Background: Plants have evolved intimate interactions with soil microbes for a range of beneficial functions including nutrient acquisition, pathogen resistance and stress tolerance. Further understanding of this system is a promising way to advance sustainable agriculture by exploiting the versatile benefits offered by the plant microbiome. The rhizosphere is the interface between plant and soil, and functions as the first step of plant defense and root microbiome recruitment. It features a specialized microbial community, intensive microbe-plant and microbe-microbe interactions, and complex signal communication. To decipher the rhizosphere microbiome assembly of soybean (Glycine max), we comprehensively characterized the soybean rhizosphere microbial community using 16S rRNA gene sequencing and evaluated the structuring influence from both host genotype and soil source. Results: Comparison of the soybean rhizosphere to bulk soil revealed significantly different microbiome composition, microbe-microbe interactions and metabolic capacity. Soil type and soybean genotype cooperatively modulated microbiome assembly with soil type predominantly shaping rhizosphere microbiome assembly while host genotype slightly tuned this recruitment process. The undomesticated progenitor species, Glycine soja, had higher rhizosphere diversity in both soil types tested in comparison to the domesticated soybean genotypes. Rhizobium, Novosphingobium, Phenylobacterium, Streptomyces, Nocardioides, etc. were robustly enriched in soybean rhizosphere irrespective of the soil tested. Co-occurrence network analysis revealed dominant soil type effects and genotype specific preferences for key microbe-microbe interactions. Functional prediction results demonstrated converged metabolic capacity in the soybean rhizosphere between soil types and among genotypes, with pathways related to xenobiotic degradation, plant-microbe interactions and nutrient transport being greatly enriched in the rhizosphere. Conclusion: This comprehensive comparison of the soybean microbiome between soil types and genotypes expands our understanding of rhizosphere microbe assembly in general and provides foundational information for soybean as a legume crop for this assembly process. The cooperative modulating role of the soil type and host genotype emphasizes the importance of integrated consideration of soil condition and plant genetic variability for future development and application of synthetic microbiomes. Additionally, the detection of the tuning role by soybean genotype in rhizosphere microbiome assembly provides a promising way for future breeding programs to integrate host traits participating in beneficial microbiota assembly. Keywords: Rhizosphere, Microbiome, Soybean genotypes, Microbe-microbe interactions, Plant-microbe network * Correspondence: 6 Department of Entomology and Plant Pathology, University of Tennessee, 154 Plant Biotechnology Building, 2505 E.J. Chapman Drive, Knoxville, TN 37996, USA Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Liu et al. BMC Microbiology (2019) 19:201 Background It has been widely recognized that plants utilize associated microbes for a range of beneficial functions including nutrient acquisition, pathogen resistance and stress tolerance [1]. Recent studies consistently demonstrate that the plant microbiome greatly extends plants’ adaptations to changing environments [2, 3]. These results suggest a promising new avenue of research for sustainable agriculture [4]. Further, microbe community assembly is not static or passive; plants can actively modulate the assembly of their beneficial microbiome in response to stressors (e.g., drought and pathogen infection). This dynamic response further highlights the possibility of optimizing crop yields by exploiting beneficial plant-microbe interactions [2, 5, 6]. The rhizosphere is an interface between plant root and soil characterized by a dynamic microbial community with intensive microbe-microbe and plant-microbe communication mediated by plant molecular signals, especially secondary metabolites [7]. At this root-microbe interface, plant and microbes have evolved intimate interactions. Plants allocate a significant portion of photosynthates as root exudates that serve as resources for microbes, and in return, microbes help to increase plant fitness via various plant growth promoting impacts [4, 8]. The rhizosphere is also the first line of plant defense to pathogen infection [1] and acts as the initial filter for the subset of microbes that will colonize the root as endophytes [9]. Understanding the major factors that shape the rhizosphere microbiome assembly and the mechanisms of mutual adaptation between microbes and plants in response to changing environmental conditions will help to identify potential targets for future crop breeding and management. Comprehensive characterization and comparison of rhizosphere microbiomes among numerous plant species under different conditions has consistently revealed the crucial impacts of soil source [9, 10] and plant genetic traits [11–13] on rhizosphere microbiome assembly. The pool of microbes available in the soil determines the initial microbial repertoire for this assembly process [7]. In addition, soil physio-chemical characteristics directly modulate microbial communities and may also indirectly alter rhizosphere microbiome assembly through impacts on host plant physiology [7]. Plant physiology and genetics also control rhizosphere composition. Differences in root morphology and in the quantity and quality of rhizodeposits could greatly diversify the composition and activity of the rhizosphere microbiome in a species-specific way [7]. With the advantage of nitrogen fixation by rhizobia, the root exudates of legumes differs from nonlegumes in both quantity and quality, with higher exudation amounts and lower carbon-to-nitrogen ratios [14]. This special trait of legumes may shape rhizosphere microbiome assembly differently co (...truncated)