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      Rhizosphere protists are key determinants of plant health

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          Abstract

          Background

          Plant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth. However, most rhizosphere microbiome research has focused on fractions of this microbiome, particularly bacteria and fungi. It remains unknown how other microbial components, especially key microbiome predators—protists—are linked to plant health. Here, we investigated the holistic rhizosphere microbiome including bacteria, microbial eukaryotes (fungi and protists), as well as functional microbial metabolism genes. We investigated these communities and functional genes throughout the growth of tomato plants that either developed disease symptoms or remained healthy under field conditions.

          Results

          We found that pathogen dynamics across plant growth is best predicted by protists. More specifically, communities of microbial-feeding phagotrophic protists differed between later healthy and diseased plants at plant establishment. The relative abundance of these phagotrophs negatively correlated with pathogen abundance across plant growth, suggesting that predator-prey interactions influence pathogen performance. Furthermore, phagotrophic protists likely shifted bacterial functioning by enhancing pathogen-suppressing secondary metabolite genes involved in mitigating pathogen success.

          Conclusions

          We illustrate the importance of protists as top-down controllers of microbiome functioning linked to plant health. We propose that a holistic microbiome perspective, including bacteria and protists, provides the optimal next step in predicting plant performance.

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          Most cited references39

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Soil networks become more connected and take up more carbon as nature restoration progresses

            Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered.
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              Establishing Causality: Opportunities of Synthetic Communities for Plant Microbiome Research.

              Plant microbiome research highlights the importance of indigenous microbial communities for host phenotypes such as growth and health. It aims to discover the molecular basis by which host-microbe and microbe-microbe interactions shape and maintain microbial communities and to understand the role of individual microorganisms, as well as their collective ecosystem function. Here, we discuss reductionist approaches to disentangle the inherent complexity of interactions in situ. Experimentally tractable, synthetic communities enable testing of hypotheses by targeted manipulation in gnotobiotic systems. Modifications of microbial, host, and environmental parameters allow for the quantitative assessment of host and microbe characteristics with dynamic and spatial resolution. We summarize first insights from this emerging field and discuss current challenges and limitations. Using multifaceted approaches to detect interactions and functions will provide new insights into the fundamental biology of plant-microbe interactions and help to harness the power of the microbiome.
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                Author and article information

                Contributors
                weizhong@njau.edu.cn
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                3 March 2020
                3 March 2020
                2020
                : 8
                : 27
                Affiliations
                [1 ]GRID grid.27871.3b, ISNI 0000 0000 9750 7019, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Key Lab of Plant Immunity, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving fertilizers, , Nanjing Agricultural University, ; Nanjing, 210095 Jiangsu People’s Republic of China
                [2 ]GRID grid.5477.1, ISNI 0000000120346234, Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, , Utrecht University, ; Padualaan 8, 3584 CH Utrecht, The Netherlands
                [3 ]GRID grid.418375.c, ISNI 0000 0001 1013 0288, Department of Terrestrial Ecology, , Netherlands Institute for Ecology (NIOO-KNAW), ; 6708 PB Wageningen, The Netherlands
                [4 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Laboratory of Nematology, , Wageningen University & Research, ; 6700 ES Wageningen, The Netherlands
                Author information
                http://orcid.org/0000-0003-0734-727X
                Article
                799
                10.1186/s40168-020-00799-9
                7055055
                32127034
                aeba39f3-e0c7-402d-ae3d-a96ac44ae984
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 21 October 2019
                : 5 February 2020
                Funding
                Funded by: National Key Research and Development Program of China
                Award ID: (2018YFD1000800)
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100012166, National Basic Research Program of China (973 Program);
                Award ID: 2015CB150500
                Award Recipient :
                Funded by: NWO-VENI grant from the Netherlands Organisation for Scientific Research
                Award ID: 016.Veni.181.078
                Award Recipient :
                Funded by: NWO grant from the Netherlands Organisation for Scientific Research
                Award ID: ALWGR.2017.016
                Award Recipient :
                Funded by: the National Natural Science Foundation of China
                Award ID: (41922053)
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                rhizosphere,pathogen of ralstonia solanacearum,protists,predator-prey interactions,secondary metabolite genes,plant health

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