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Title: Differences in resource use lead to coexistence of seed-transmitted microbial populations

Abstract

Seeds are involved in the vertical transmission of microorganisms in plants and act as reservoirs for the plant microbiome. They could serve as carriers of pathogens, making the study of microbial interactions on seeds important in the emergence of plant diseases. We studied the influence of biological disturbances caused by seed transmission of two phytopathogenic agents, Alternaria brassicicola Abra43 (Abra43) and Xanthomonas campestris pv. campestris 8004 (Xcc8004), on the structure and function of radish seed microbial assemblages, as well as the nutritional overlap between Xcc8004 and the seed microbiome, to find seed microbial residents capable of outcompeting this pathogen. According to taxonomic and functional inference performed on metagenomics reads, no shift in structure and function of the seed microbiome was observed following Abra43 and Xcc8004 transmission. This lack of impact derives from a limited overlap in nutritional resources between Xcc8004 and the major bacterial populations of radish seeds. However, two native seed-associated bacterial strains belonging to Stenotrophomonas rhizophila displayed a high overlap with Xcc8004 regarding the use of resources; they might therefore limit its transmission. The strategy we used may serve as a foundation for the selection of seed indigenous bacterial strains that could limit seed transmission of pathogens.

Authors:
 [1]; ORCiD logo [2];  [3];  [1];  [2];  [1];  [1];  [4];  [4]; ORCiD logo [2];  [1]
  1. French National Inst. for Agricultural Research (INRA), Baeucouze (France)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Austrian Inst. of Technology, Tulln (Austria)
  4. French National Inst. for Agricultural Research (INRA), Castanet-Tolosan (France)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1546502
Alternate Identifier(s):
OSTI ID: 1561670
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Torres-Cortes, G., Garcia, Benjamin J., Compant, S., Rezki, S., Jones, Piet C., Preveaux, A., Briand, M., Roulet, A., Bouchez, O., Jacobson, Daniel A., and Barret, Mattieu. Differences in resource use lead to coexistence of seed-transmitted microbial populations. United States: N. p., 2019. Web. doi:10.1038/s41598-019-42865-9.
Torres-Cortes, G., Garcia, Benjamin J., Compant, S., Rezki, S., Jones, Piet C., Preveaux, A., Briand, M., Roulet, A., Bouchez, O., Jacobson, Daniel A., & Barret, Mattieu. Differences in resource use lead to coexistence of seed-transmitted microbial populations. United States. doi:10.1038/s41598-019-42865-9.
Torres-Cortes, G., Garcia, Benjamin J., Compant, S., Rezki, S., Jones, Piet C., Preveaux, A., Briand, M., Roulet, A., Bouchez, O., Jacobson, Daniel A., and Barret, Mattieu. Tue . "Differences in resource use lead to coexistence of seed-transmitted microbial populations". United States. doi:10.1038/s41598-019-42865-9. https://www.osti.gov/servlets/purl/1546502.
@article{osti_1546502,
title = {Differences in resource use lead to coexistence of seed-transmitted microbial populations},
author = {Torres-Cortes, G. and Garcia, Benjamin J. and Compant, S. and Rezki, S. and Jones, Piet C. and Preveaux, A. and Briand, M. and Roulet, A. and Bouchez, O. and Jacobson, Daniel A. and Barret, Mattieu},
abstractNote = {Seeds are involved in the vertical transmission of microorganisms in plants and act as reservoirs for the plant microbiome. They could serve as carriers of pathogens, making the study of microbial interactions on seeds important in the emergence of plant diseases. We studied the influence of biological disturbances caused by seed transmission of two phytopathogenic agents, Alternaria brassicicola Abra43 (Abra43) and Xanthomonas campestris pv. campestris 8004 (Xcc8004), on the structure and function of radish seed microbial assemblages, as well as the nutritional overlap between Xcc8004 and the seed microbiome, to find seed microbial residents capable of outcompeting this pathogen. According to taxonomic and functional inference performed on metagenomics reads, no shift in structure and function of the seed microbiome was observed following Abra43 and Xcc8004 transmission. This lack of impact derives from a limited overlap in nutritional resources between Xcc8004 and the major bacterial populations of radish seeds. However, two native seed-associated bacterial strains belonging to Stenotrophomonas rhizophila displayed a high overlap with Xcc8004 regarding the use of resources; they might therefore limit its transmission. The strategy we used may serve as a foundation for the selection of seed indigenous bacterial strains that could limit seed transmission of pathogens.},
doi = {10.1038/s41598-019-42865-9},
journal = {Scientific Reports},
number = 1,
volume = 9,
place = {United States},
year = {2019},
month = {4}
}

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Works referenced in this record:

Selection on soil microbiomes reveals reproducible impacts on plant function
journal, October 2014

  • Panke-Buisse, Kevin; Poole, Angela C.; Goodrich, Julia K.
  • The ISME Journal, Vol. 9, Issue 4
  • DOI: 10.1038/ismej.2014.196

Rapid responses of soil microorganisms improve plant fitness in novel environments
journal, August 2012

  • Lau, J. A.; Lennon, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
  • DOI: 10.1073/pnas.1202319109

Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria
journal, May 2011


Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities
journal, February 2013

  • Sugiyama, Akifumi; Bakker, Matthew G.; Badri, Dayakar V.
  • Botany, Vol. 91, Issue 2
  • DOI: 10.1139/cjb-2012-0217

Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

Ecological Succession and Stochastic Variation in the Assembly of Arabidopsis thaliana Phyllosphere Communities
journal, December 2013


Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015

  • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1414592112

Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus
journal, November 2016

  • Leff, Jonathan W.; Lynch, Ryan C.; Kane, Nolan C.
  • New Phytologist, Vol. 214, Issue 1
  • DOI: 10.1111/nph.14323

Ecological patterns of seed microbiome diversity, transmission, and assembly
journal, June 2017

  • Shade, Ashley; Jacques, Marie-Agnès; Barret, Matthieu
  • Current Opinion in Microbiology, Vol. 37
  • DOI: 10.1016/j.mib.2017.03.010

Cytokinins and the bacterial symbiosis of Ardisia species
journal, November 1972

  • Rodrigues Pereira, A. S.; Houwen, P. J. W.; Deurenberg-Vos, H. W. J.
  • Zeitschrift für Pflanzenphysiologie, Vol. 68, Issue 2
  • DOI: 10.1016/S0044-328X(72)80166-1

A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds
journal, December 2014

  • Goggin, Danica E.; Emery, R. J. Neil; Kurepin, Leonid V.
  • Annals of Botany, Vol. 115, Issue 2
  • DOI: 10.1093/aob/mcu231

Fungal Endophyte (Epichloë festucae) Alters the Nutrient Content of Festuca rubra Regardless of Water Availability
journal, December 2013

  • Vázquez-de-Aldana, Beatriz R.; García-Ciudad, Antonia; García-Criado, Balbino
  • PLoS ONE, Vol. 8, Issue 12
  • DOI: 10.1371/journal.pone.0084539

Dynamics of Seed Transmission of Plant Pathogens
journal, September 1966


The Epidemiology and Management of Seedborne Bacterial Diseases
journal, September 2007


Contamination of bean seeds by Xanthomonas axonopodis pv. phaseoli associated with low bacterial densities in the phyllosphere under field and greenhouse conditions
journal, June 2007

  • Darrasse, Armelle; Bureau, Christine; Samson, Régine
  • European Journal of Plant Pathology, Vol. 119, Issue 2
  • DOI: 10.1007/s10658-007-9164-2

Transmission of Plant-Pathogenic Bacteria by Nonhost Seeds without Induction of an Associated Defense Reaction at Emergence
journal, August 2010

  • Darrasse, A.; Darsonval, A.; Boureau, T.
  • Applied and Environmental Microbiology, Vol. 76, Issue 20
  • DOI: 10.1128/AEM.01098-10

A New Approach to Modify Plant Microbiomes and Traits by Introducing Beneficial Bacteria at Flowering into Progeny Seeds
journal, January 2017

  • Mitter, Birgit; Pfaffenbichler, Nikolaus; Flavell, Richard
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00011

Plant microbiota affects seed transmission of phytopathogenic microorganisms: Plant microbiota affects seed transmission
journal, July 2016

  • Barret, Matthieu; Guimbaud, Jean-François; Darrasse, Armelle
  • Molecular Plant Pathology, Vol. 17, Issue 6
  • DOI: 10.1111/mpp.12382

Deciphering the Pathobiome: Intra- and Interkingdom Interactions Involving the Pathogen Erysiphe alphitoides
journal, May 2016


Differences in stability of seed-associated microbial assemblages in response to invasion by phytopathogenic microorganisms
journal, January 2016

  • Rezki, Samir; Campion, Claire; Iacomi-Vasilescu, Beatrice
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.1923

Isolation of 12 polymorphic microsatellite loci in the phytopathogenic fungus Alternaria brassicicola
journal, December 2005


The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi
journal, January 2012

  • Pochon, Stephanie; Terrasson, Emmanuel; Guillemette, Thomas
  • Plant Methods, Vol. 8, Issue 1
  • DOI: 10.1186/1746-4811-8-16

Flower infection of Brassica oleracea with Xanthomonas campestris pv. campestris results in high levels of seed infection
journal, December 2012

  • van der Wolf, J. M.; van der Zouwen, P. S.; van der Heijden, L.
  • European Journal of Plant Pathology, Vol. 136, Issue 1
  • DOI: 10.1007/s10658-012-0141-z

Fold change rank ordering statistics: a new method for detecting differentially expressed genes
journal, January 2014


Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
journal, January 2018


Comparison of 61 Sequenced Escherichia coli Genomes
journal, July 2010

  • Lukjancenko, Oksana; Wassenaar, Trudy M.; Ussery, David W.
  • Microbial Ecology, Vol. 60, Issue 4
  • DOI: 10.1007/s00248-010-9717-3

Assembly of seed-associated microbial communities within and across successive plant generations
journal, October 2017


Functional Microbial Features Driving Community Assembly During Seed Germination and Emergence
journal, June 2018

  • Torres-Cortés, Gloria; Bonneau, Sophie; Bouchez, Olivier
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00902

Terroir is a key driver of seed-associated microbial assemblages: Terroir shapes the seed microbiota
journal, August 2015

  • Klaedtke, Stephanie; Jacques, Marie-Agnès; Raggi, Lorenzo
  • Environmental Microbiology, Vol. 18, Issue 6
  • DOI: 10.1111/1462-2920.12977

Diversity of the spinach ( Spinacia oleracea ) spermosphere and phyllosphere bacterial communities
journal, August 2013

  • Lopez-Velasco, Gabriela; Carder, Phyllis A.; Welbaum, Gregory E.
  • FEMS Microbiology Letters, Vol. 346, Issue 2
  • DOI: 10.1111/1574-6968.12216

Dominant Groups of Potentially Active Bacteria Shared by Barley Seeds become Less Abundant in Root Associated Microbiome
journal, June 2017


Identification of a molecular dialogue between developing seeds of Medicago truncatula and seedborne xanthomonads
journal, April 2015

  • Terrasson, Emmanuel; Darrasse, Armelle; Righetti, Karima
  • Journal of Experimental Botany, Vol. 66, Issue 13
  • DOI: 10.1093/jxb/erv167

Small cysteine-rich antifungal proteins from radish: their role in host defense.
journal, May 1995

  • Terras, F. R.; Eggermont, K.; Kovaleva, V.
  • The Plant Cell, Vol. 7, Issue 5
  • DOI: 10.1105/tpc.7.5.573

Defence on demand: mechanisms behind optimal defence patterns
journal, September 2012

  • Meldau, Stefan; Erb, Matthias; Baldwin, Ian T.
  • Annals of Botany, Vol. 110, Issue 8
  • DOI: 10.1093/aob/mcs212

Simplified and representative bacterial community of maize roots
journal, March 2017

  • Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
  • DOI: 10.1073/pnas.1616148114

Emergence Shapes the Structure of the Seed Microbiota
journal, December 2014

  • Barret, Matthieu; Briand, Martial; Bonneau, Sophie
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03722-14

Microbial Dynamics and Interactions in the Spermosphere
journal, September 2004


Bacterial competition: surviving and thriving in the microbial jungle
journal, November 2009

  • Hibbing, Michael E.; Fuqua, Clay; Parsek, Matthew R.
  • Nature Reviews Microbiology, Vol. 8, Issue 1
  • DOI: 10.1038/nrmicro2259

Historical Contingency in Community Assembly: Integrating Niches, Species Pools, and Priority Effects
journal, December 2015


Using Ecology, Physiology, and Genomics to Understand Host Specificity in Xanthomonas
journal, August 2016


Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere
journal, May 2012

  • Schmidt, Christoph Stephan; Alavi, Mohamadali; Cardinale, Massimiliano
  • Biology and Fertility of Soils, Vol. 48, Issue 8
  • DOI: 10.1007/s00374-012-0688-z

The seed microbiome: Origins, interactions, and impacts
journal, May 2017


Functional overlap of the Arabidopsis leaf and root microbiota
journal, December 2015

  • Bai, Yang; Müller, Daniel B.; Srinivas, Girish
  • Nature, Vol. 528, Issue 7582
  • DOI: 10.1038/nature16192

Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Genome Sequence of the Necrotrophic Plant Pathogen Alternaria brassicicola Abra43
journal, February 2018

  • Belmas, Elodie; Briand, Martial; Kwasiborski, Anthony
  • Genome Announcements, Vol. 6, Issue 6
  • DOI: 10.1128/genomeA.01559-17

Kraken: ultrafast metagenomic sequence classification using exact alignments
journal, January 2014


phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

Prokka: rapid prokaryotic genome annotation
journal, March 2014


Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences
journal, November 2015

  • Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1248

The Sequence Alignment/Map format and SAMtools
journal, June 2009


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Bacterial niches inside seeds of Cucumis melo L.
journal, January 2017


The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set
journal, September 1999


Niches and routes of transmission of Xanthomonas citri pv. fuscans to bean seeds
journal, July 2017


Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms
journal, January 1993