Stimulation of distinct rhizosphere bacteria drives phosphorus and nitrogen mineralization in oilseed rape under field conditions

Lidbury, Ian D. E. A., Raguideau, Sebastien, Borsetto, Chiara, Murphy, Andrew R. J., Bottrill, Andrew, Liu, Senlin, Stark, Richard, Fraser, Tandra, Goodall, Andrew, Jones, Alex, Bending, Gary D., Tibbet, Mark, Hammond, John P., Quince, Chris, Scanlan, David J., Pandhal, Jagroop and Wellington, Elizabeth M. H. (2022) Stimulation of distinct rhizosphere bacteria drives phosphorus and nitrogen mineralization in oilseed rape under field conditions. mSystems, 7 (4). ISSN 2379-5077

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Abstract

Advances in DNA sequencing technologies have drastically changed our perception of the structure and complexity of the plant microbiome. By comparison, our ability to accurately identify the metabolically active fraction of soil microbiota and its specific functional role in augmenting plant health is relatively limited. Important ecological interactions being performed by microbes can be investigated by analyzing the extracellular protein fraction. Here, we combined a unique protein extraction method and an iterative bioinformatics pipeline to capture and identify extracellular proteins (metaexoproteomics) synthesized in the rhizosphere of Brassica spp. We first validated our method in the laboratory by successfully identifying proteins related to a host plant (Brassica rapa) and its bacterial inoculant, Pseudomonas putida BIRD-1. This identified numerous rhizosphere specific proteins linked to the acquisition of plant-derived nutrients in P. putida. Next, we analyzed natural field-soil microbial communities associated with Brassica napus L. (oilseed rape). By combining metagenomics with metaexoproteomics, 1,885 plant, insect, and microbial proteins were identified across bulk and rhizosphere samples. Metaexoproteomics identified a significant shift in the metabolically active fraction of the soil microbiota responding to the presence of B. napus roots that was not apparent in the composition of the total microbial community (metagenome). This included stimulation of rhizosphere-specialized bacteria, such as Gammaproteobacteria, Betaproteobacteria, and Flavobacteriia, and the upregulation of plant beneficial functions related to phosphorus and nitrogen mineralization. Our metaproteomic assessment of the “active” plant microbiome at the field-scale demonstrates the importance of moving beyond metagenomics to determine ecologically important plant-microbe interactions underpinning plant health.

Item Type: Article
Additional Information: Funding Information: This study was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) and National Environmental Research Council (NERC) under project codes BB/ L026074/1, BB/T009152/1 and NE/S013539/1 linked to The Soil and Rhizosphere Interactions for Sustainable Agri-ecosystems (SARISA) program and a Discovery Fellowship (to I.D.E.A.L.) and NERC Environmental 'Omics Synthesis Grant (to I.D.E.A.L., J.P., and E.M.H.W.), respectively. We declare no competing interests.
Uncontrolled Keywords: brassica napus,field soil,metagenomics,metaproteomics,plant microbiome,sustainable agriculture,microbiology,physiology,biochemistry,ecology, evolution, behavior and systematics,modelling and simulation,molecular biology,genetics,computer science applications ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 09 Sep 2022 09:30
Last Modified: 04 Oct 2022 00:21
URI: https://ueaeprints.uea.ac.uk/id/eprint/88011
DOI: 10.1128/msystems.00025-22

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