Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics

Vittorio Tracanna; Adam Ossowicki; Marloes L.C. Petrus; Sam Overduin; Barbara R. Terlouw; George Lund; Serina L. Robinson; Sven Warris; Elio G.W.M. Schijlen; Gilles P. van Wezel; J.M. Raaijmakers; Paolina Garbeva; Marnix H. Medema

doi:10.1128/mSystems.01116-20

Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics

Vittorio Tracanna, Adam Ossowicki, Marloes L.C. Petrus, Sam Overduin, Barbara R. Terlouw, George Lund, Serina L. Robinson, Sven Warris, Elio G.W.M. Schijlen, Gilles P. van Wezel, J.M. Raaijmakers, Paolina Garbeva (Corresponding author), Marnix H. Medema (Corresponding author)

NIOO - Microbial Ecology (ME)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

32 Citations (Scopus)

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Abstract

Disease-suppressive soils protect plants against soilborne fungal pathogens that would otherwise cause root infections. Soil suppressiveness is, in most cases, mediated by the antagonistic activity of the microbial community associated with the plant roots. Considering the enormous taxonomic and functional diversity of the root-associated microbiome, identification of the microbial genera and mechanisms underlying this phenotype is challenging. One approach to unravel the underlying mechanisms is to identify metabolic pathways enriched in the disease-suppressive microbial community, in particular, pathways that harbor natural products with antifungal properties. An important class of these natural products includes peptides produced by nonribosomal peptide synthetases (NRPSs). Here, we applied functional amplicon sequencing of NRPS-associated adenylation domains (A domains) to a collection of eight soils that are suppressive or nonsuppressive (i.e., conducive) to Fusarium culmorum, a fungal root pathogen of wheat. To identify functional elements in the root-associated bacterial community, we developed an open-source pipeline, referred to as dom2BGC, for amplicon annotation and putative gene cluster reconstruction through analyzing A domain co-occurrence across samples. We applied this pipeline to rhizosphere communities from four disease-suppressive and four conducive soils and found significant similarities in NRPS repertoires between suppressive soils. Specifically, several siderophore biosynthetic gene clusters were consistently associated with suppressive soils, hinting at competition for iron as a potential mechanism of suppression. Finally, to validate dom2BGC and to allow more unbiased functional metagenomics, we performed 10x metagenomic sequencing of one suppressive soil, leading to the identification of multiple gene clusters potentially associated with the disease-suppressive phenotype.

Original language	English
Article number	e01116-20
Journal	mSystems
Volume	6
Issue number	3
DOIs	https://doi.org/10.1128/mSystems.01116-20
Publication status	Published - 2021

Keywords

international
Plan_S-Compliant-OA

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7184_TracannaFinal published version, 2.55 MBLicence: CC BY

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Tracanna, V., Ossowicki, A., Petrus, M. L. C., Overduin, S., Terlouw, B. R., Lund, G., Robinson, S. L., Warris, S., Schijlen, E. G. W. M., van Wezel, G. P., Raaijmakers, J. M., Garbeva, P., & Medema, M. H. (2021). Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics. mSystems, 6(3), Article e01116-20. https://doi.org/10.1128/mSystems.01116-20

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title = "Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics",

abstract = "Disease-suppressive soils protect plants against soilborne fungal pathogens that would otherwise cause root infections. Soil suppressiveness is, in most cases, mediated by the antagonistic activity of the microbial community associated with the plant roots. Considering the enormous taxonomic and functional diversity of the root-associated microbiome, identification of the microbial genera and mechanisms underlying this phenotype is challenging. One approach to unravel the underlying mechanisms is to identify metabolic pathways enriched in the disease-suppressive microbial community, in particular, pathways that harbor natural products with antifungal properties. An important class of these natural products includes peptides produced by nonribosomal peptide synthetases (NRPSs). Here, we applied functional amplicon sequencing of NRPS-associated adenylation domains (A domains) to a collection of eight soils that are suppressive or nonsuppressive (i.e., conducive) to Fusarium culmorum, a fungal root pathogen of wheat. To identify functional elements in the root-associated bacterial community, we developed an open-source pipeline, referred to as dom2BGC, for amplicon annotation and putative gene cluster reconstruction through analyzing A domain co-occurrence across samples. We applied this pipeline to rhizosphere communities from four disease-suppressive and four conducive soils and found significant similarities in NRPS repertoires between suppressive soils. Specifically, several siderophore biosynthetic gene clusters were consistently associated with suppressive soils, hinting at competition for iron as a potential mechanism of suppression. Finally, to validate dom2BGC and to allow more unbiased functional metagenomics, we performed 10x metagenomic sequencing of one suppressive soil, leading to the identification of multiple gene clusters potentially associated with the disease-suppressive phenotype.",

keywords = "international, Plan_S-Compliant-OA",

author = "Vittorio Tracanna and Adam Ossowicki and Petrus, {Marloes L.C.} and Sam Overduin and Terlouw, {Barbara R.} and George Lund and Robinson, {Serina L.} and Sven Warris and Schijlen, {Elio G.W.M.} and {van Wezel}, {Gilles P.} and J.M. Raaijmakers and Paolina Garbeva and Medema, {Marnix H.}",

note = "7184, ME; Data archiving: data archived in NCBI (no NIOO data)",

year = "2021",

doi = "10.1128/mSystems.01116-20",

language = "English",

volume = "6",

journal = "mSystems",

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T1 - Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics

AU - Tracanna, Vittorio

AU - Ossowicki, Adam

AU - Petrus, Marloes L.C.

AU - Overduin, Sam

AU - Terlouw, Barbara R.

AU - Lund, George

AU - Robinson, Serina L.

AU - Warris, Sven

AU - Schijlen, Elio G.W.M.

AU - van Wezel, Gilles P.

AU - Raaijmakers, J.M.

AU - Garbeva, Paolina

AU - Medema, Marnix H.

N1 - 7184, ME; Data archiving: data archived in NCBI (no NIOO data)

PY - 2021

Y1 - 2021

N2 - Disease-suppressive soils protect plants against soilborne fungal pathogens that would otherwise cause root infections. Soil suppressiveness is, in most cases, mediated by the antagonistic activity of the microbial community associated with the plant roots. Considering the enormous taxonomic and functional diversity of the root-associated microbiome, identification of the microbial genera and mechanisms underlying this phenotype is challenging. One approach to unravel the underlying mechanisms is to identify metabolic pathways enriched in the disease-suppressive microbial community, in particular, pathways that harbor natural products with antifungal properties. An important class of these natural products includes peptides produced by nonribosomal peptide synthetases (NRPSs). Here, we applied functional amplicon sequencing of NRPS-associated adenylation domains (A domains) to a collection of eight soils that are suppressive or nonsuppressive (i.e., conducive) to Fusarium culmorum, a fungal root pathogen of wheat. To identify functional elements in the root-associated bacterial community, we developed an open-source pipeline, referred to as dom2BGC, for amplicon annotation and putative gene cluster reconstruction through analyzing A domain co-occurrence across samples. We applied this pipeline to rhizosphere communities from four disease-suppressive and four conducive soils and found significant similarities in NRPS repertoires between suppressive soils. Specifically, several siderophore biosynthetic gene clusters were consistently associated with suppressive soils, hinting at competition for iron as a potential mechanism of suppression. Finally, to validate dom2BGC and to allow more unbiased functional metagenomics, we performed 10x metagenomic sequencing of one suppressive soil, leading to the identification of multiple gene clusters potentially associated with the disease-suppressive phenotype.

AB - Disease-suppressive soils protect plants against soilborne fungal pathogens that would otherwise cause root infections. Soil suppressiveness is, in most cases, mediated by the antagonistic activity of the microbial community associated with the plant roots. Considering the enormous taxonomic and functional diversity of the root-associated microbiome, identification of the microbial genera and mechanisms underlying this phenotype is challenging. One approach to unravel the underlying mechanisms is to identify metabolic pathways enriched in the disease-suppressive microbial community, in particular, pathways that harbor natural products with antifungal properties. An important class of these natural products includes peptides produced by nonribosomal peptide synthetases (NRPSs). Here, we applied functional amplicon sequencing of NRPS-associated adenylation domains (A domains) to a collection of eight soils that are suppressive or nonsuppressive (i.e., conducive) to Fusarium culmorum, a fungal root pathogen of wheat. To identify functional elements in the root-associated bacterial community, we developed an open-source pipeline, referred to as dom2BGC, for amplicon annotation and putative gene cluster reconstruction through analyzing A domain co-occurrence across samples. We applied this pipeline to rhizosphere communities from four disease-suppressive and four conducive soils and found significant similarities in NRPS repertoires between suppressive soils. Specifically, several siderophore biosynthetic gene clusters were consistently associated with suppressive soils, hinting at competition for iron as a potential mechanism of suppression. Finally, to validate dom2BGC and to allow more unbiased functional metagenomics, we performed 10x metagenomic sequencing of one suppressive soil, leading to the identification of multiple gene clusters potentially associated with the disease-suppressive phenotype.

KW - international

KW - Plan_S-Compliant-OA

U2 - 10.1128/mSystems.01116-20

DO - 10.1128/mSystems.01116-20

M3 - Article

SN - 2379-5077

VL - 6

JO - mSystems

JF - mSystems

IS - 3

M1 - e01116-20

ER -

Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10X metagenomics

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