Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale

Pauline Bernardo; Tristan Charles-Dominique; Mohamed Barakat; Philippe Ortet; Emmanuel Fernandez; Denis Filloux; Penelope Hartnady; Tony Rebelo; Stephen Cousins; François Mesléard; Damien Cohez; Nicole Yavercovski; Arvind Varsani; Gordon Harkins; Michel Peterschmitt; Carolyn Malmstrom; Darren Martin; Philippe Roumagnac

Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale

Pauline Bernardo ¹ Tristan Charles-Dominique ^{2, 3} Mohamed Barakat ^{4, 5} Philippe Ortet ^{4, 5} Emmanuel Fernandez ⁶ Denis Filloux ¹ Penelope Hartnady Tony Rebelo Stephen Cousins François Mesléard ^{7, 8, 9} Damien Cohez ¹⁰ Nicole Yavercovski ⁷ Arvind Varsani ¹¹ Gordon Harkins Michel Peterschmitt ¹ Carolyn Malmstrom Darren Martin Philippe Roumagnac ⁶

1 UMR BGPI - Biologie et Génétique des Interactions Plante-Parasite

2 Xishuangbanna Tropical Botanical Garden

3 Kirstenbosch Research Centre

4 BIAM - Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB)

5 LEMIRE - Laboratoire d'Ecologie Microbienne de la Rhizosphère et d'Environnements Extrêmes

BIAM - Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB) : DRF/BIAM

6 CIRAD - Centre de Coopération Internationale en Recherche Agronomique pour le Développement

7 Centre de recherche de la Tour du Valat

8 AMU - Aix Marseille Université

9 IMBE - Institut méditerranéen de biodiversité et d'écologie marine et continentale

10 Station Biologique de la Tour du Valat

11 Electron Microscopy Unit

Abstract : Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km 2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature.

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Journal articles

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Environmental Sciences

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Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale

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