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Plant Rhizosphere Selection of Plasmodiophorid Lineages from Bulk Soil : the Importance of “Hidden” Diversity

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Plant Rhizosphere Selection of Plasmodiophorid Lineages from Bulk Soil : the Importance of “Hidden” Diversity Original citation: Bass, David, van der Gast, Christopher, Thomson, Serena K., Neuhauser, Sigrid, Hilton, Sally and Bending, G. D.. (2018) Plant rhizosphere selection of Plasmodiophorid lineages from bulk soil : the importance of “hidden” diversity. Frontiers in Microbiology, 9. 168. Permanent WRAP URL: http://wrap.warwick.ac.uk/99174 Copyright and reuse: The Warwick Research Archive Portal (WRAP) makes this work of researchers of the University of Warwick available open access under the following conditions. This article is made available under the Creative Commons Attribution 4.0 International license (CC BY 4.0) and may be reused according to the conditions of the license. For more details see: http://creativecommons.org/licenses/by/4.0/ A note on versions: The version presented in WRAP is the published version, or, version of record, and may be cited as it appears here. For more information, please contact the WRAP Team at: [email protected] warwick.ac.uk/lib-publications ORIGINAL RESEARCH published: 13 February 2018 doi: 10.3389/fmicb.2018.00168 Plant Rhizosphere Selection of Plasmodiophorid Lineages from Bulk Soil: The Importance of “Hidden” Diversity David Bass 1,2*, Christopher van der Gast 3, Serena Thomson 4, Sigrid Neuhauser 5, Sally Hilton 4 and Gary D. Bending 4 1 Department of Life Sciences, Natural History Museum, London, United Kingdom, 2 Centre for Environment, Fisheries and Aquaculture Science, Weymouth, United Kingdom, 3 School of Healthcare Science, Manchester Metropolitan University, Manchester, United Kingdom, 4 School of Life Sciences, University of Warwick, Coventry, United Kingdom, 5 Institute of Microbiology, University of Innsbruck, Innsbruck, Austria Microbial communities closely associated with the rhizosphere can have strong positive and negative impacts on plant health and growth. We used a group-specific amplicon approach to investigate local scale drivers in the diversity and distribution of plasmodiophorids in rhizosphere/root and bulk soil samples from oilseed rape (OSR) and Edited by: wheat agri-systems. Plasmodiophorids are plant- and stramenopile-associated protists Davide Bulgarelli, including well known plant pathogens as well as symptomless endobiotic species. We University of Dundee, United Kingdom detected 28 plasmodiophorid lineages (OTUs), many of them novel, and showed that Reviewed by: plasmodiophorid communities were highly dissimilar and significantly divergent between Collin M. Timm, Johns Hopkins University, wheat and OSR rhizospheres and between rhizosphere and bulk soil samples. Bulk United States soil communities were not significantly different between OSR and wheat systems. Peter Thorpe, James Hutton Institute, Wheat and OSR rhizospheres selected for different plasmodiophorid lineages. An OTU United Kingdom corresponding to Spongospora nasturtii was positively selected in the OSR rhizosphere, *Correspondence: as were two genetically distinct OTUs. Two novel lineages related to Sorosphaerula David Bass veronicae were significantly associated with wheat rhizosphere samples, indicating [email protected] unknown plant-protist relationships. We show that group-targeted eDNA approaches to Specialty section: microbial symbiont-host ecology reveal significant novel diversity and enable inference This article was submitted to of differential activity and potential interactions between sequence types, as well as their Plant Microbe Interactions, a section of the journal presence. Frontiers in Microbiology Keywords: plasmodiophorid, Plasmodiophora, rhizosphere, oilseed rape, wheat, eDNA, soil Received: 05 July 2017 Accepted: 25 January 2018 Published: 13 February 2018 INTRODUCTION Citation: Bass D, van der Gast C, Thomson S, Plant roots release considerable amounts of labile exudates and debris into the soil, which results Neuhauser S, Hilton S and in intense microbial activity in the rhizosphere soil which surrounds roots, and the selection of Bending GD (2018) Plant Rhizosphere communities which are structurally and functionally distinct from the bulk soil (Morgan et al., Selection of Plasmodiophorid Lineages from Bulk Soil: The 2005) The rhizosphere microbiome can have major impacts on plant growth and nutrition, which Importance of “Hidden” Diversity. can be both positive and negative, through complex direct and indirect interactions. Although it Front. Microbiol. 9:168. is widely appreciated that a broad range of microbial groups can inhabit the rhizosphere, most doi: 10.3389/fmicb.2018.00168 studies have focussed on bacteria and fungi (Mendes et al., 2013; Philippot et al., 2013). For Frontiers in Microbiology | www.frontiersin.org 1 February 2018 | Volume 9 | Article 168 Bass et al. Plasmodiophorid Diversity and Selection in Plant Rhizospheres these groups, a range of factors can determine the specific sporangial infections in hosts within the plant families Poaceae, communities which assemble in the rhizosphere, including Brassicaceae, Leguminosae and Geraniaceae (Qu and Christ, plant characteristics such as genotype and age, environmental 2006). Polymyxa graminis, which has primary hosts including properties including soil type and climate, and in agricultural most Poaceae, can for example also infect Arabidopsis thaliana soils, management interventions such as crop rotation and as alternative host (Smith et al., 2011). Similarly, Polymyxa fertilization (Bennett et al., 2012). Protists are also components betae, which was considered to be a specialist pathogen of of the rhizosphere microbiome (Mendes et al., 2013), and can Chenopodiaceae (Desoignies et al., 2014), has now been found also have marked impacts on plant growth through direct and to also infect graminaceaous hosts such as wheat (Smith et al., indirect pathways (Bonkowski, 2004). However, they are typically 2013). not considered in studies of rhizosphere microbiology, largely The complexity of the plasmodiophorid life cycle (Bulman because culture independent techniques to profile complex and Neuhauser, 2017), coupled with their small size (3–6 µm), protist communities remain limited (Adl et al., 2014), with the makes them difficult to study. Specimen-independent molecular result that there is little understanding of the factors which shape probing and sequencing of microbial diversity in environmental protist communities in the rhizosphere. samples, referred to as eDNA (environmental DNA) offers There is one protist group in particular—plasmodiophorids— an alternative perspective on elusive and cryptic microbes to that rarely receive attention in rhizosphere ecology studies more classical organism-centric studies (Bass et al., 2015). yet are well known as plant pathogens and virus vectors. A recent eDNA study (Neuhauser et al., 2014) investigated Plasmodiophorids (Rhizaria; Endomyxa; class Phytomyxea, plasmodiophorid biodiversity by analysing root and soil- Order Plasmodiophorida) are parasites and symbionts of associated plasmodiophorids in a range of habitats, including angiosperms and stramenopiles (Bass et al., 2009; Neuhauser a vineyard, flood plain and glacier forefield. Eighty-one new et al., 2014). Plasmodiophorid diversity is much greater than OTUs were discovered from just 6 locations, significantly adding the few known parasitic taxa and their broader role(s) in the to the 41 known phytomyxid (combined plasmodiophorid and rhizosphere are of great interest. Plasmodiophorids form obligate phagomyxid) lineages. This suggests that many lineages remain associations with their hosts, which are often green plants, but uncharacterized, the biological function of which is unknown. in some instances, they can also infect other parasites including Given the importance of plasmodiophorids as crop disease heterotrophic stramenopiles, e.g., Woronina pythii, which infects agents and viral disease vectors, understanding the recently Pythium spp. (Dylewski and Miller, 1983; Neuhauser et al., demonstrated “expanded” diversity and distribution of the group 2014). Plasmodiophorids are the causative agents of economically within agricultural systems is important to more fully understand significant diseases of crops including brassicas, potatoes, and crop health, parasite load, and organismal interactions. grain crops (e.g., maize, rice, wheat, sorghum). Plasmodiophora A novel insight into the structure of plasmodiophorid brassicae is the commercially most important and best studied communities and the factors modulating this can be deduced plasmodiophorid, causing clubroot disease in cruciferous plants by objectively partitioning the community into core and such as oilseed rape (OSR). Clubroot has been shown to result satellite taxa (van der Gast et al., 2011). By decomposing in average crop losses of 10-15% on a global scale (Dixon, the relationship between distribution (number of sample 2009, 2014; Hwang et al., 2012). Other plasmodiophorids include communities that taxa occupy) and mean abundance Spongospora subterranea, which causes powdery scab of potato (across those sample communities), core members of the and can also vector Potato Mop Top Virus (Beuch et al., plasmodiophorid communities can be identified as those that 2015; Falloon et al., 2015). Polymxa graminis can infect most are locally abundant and non-randomly distributed. With graminaceous crops where it does not cause disease symptoms the rare satellite taxa defined as those that are typically in itself, but can transmit several viruses, such as soil-borne wheat low abundance and randomly distributed through sample mosaic virus (SBWMV), which is considered as
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