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Pseudomonas fluorescens C7R12 type III secretion system impacts mycorrhization of Medicago truncatula and associated microbial communities

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Abstract

Type three secretion systems (T3SSs) mediate cell-to-cell interactions between Gram-negative bacteria and eukaryotes. We hypothesized that fluorescent pseudomonads harboring T3SS (T3SS+) would be beneficial to arbuscular mycorrhizal symbiosis because non-pathogenic fluorescent pseudomonads have been previously shown to be much more abundant in mycorrhizal than in non-mycorrhizal roots. We tested this hypothesis by comparing mycorrhization and the associated rhizosphere microbial communities of Medicago truncatula grown in a non-sterile soil inoculated with either the T3SS+ mycorrhiza helper bacterium Pseudomonas fluorescens (C7R12) or a T3SS− mutant of the strain. Results showed that the bacterial secretion system was responsible for the promotion of mycorrhization because root colonization by arbuscular mycorrhizal fungi was not promoted by the T3SS− mutant. The observed T3SS-mediated promotion of mycorrhization was associated with changes in the rhizosphere bacterial communities and the increased occurrence of Claroidoglomeraceae within the intraradical arbuscular mycorrhizal fungi. Furthermore, both pseudomonad strains promoted the host-free growth of a model arbuscular mycorrhizal fungus in vitro, suggesting that T3SS-mediated promotion of mycorrhization occurs during plant-fungal interactions rather than during the pre-symbiotic phase of fungal growth. Taken together, these data provide evidence for the involvement of T3SS in promoting arbuscular mycorrhization by a model fluorescent pseudomonad and suggest the implication of interactions between the bacterium and mycorrhizas.

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Acknowledgments

This work was funded by the Regional Council of Burgundy, RCB (Dijon, France), and supported by a doctoral grant to A. Viollet by “Conseil Régional de Bourgogne” and INRA (EA, SPE). The authors are grateful to Thérèse Corberand, Catherine Barraud, and Jerôme Manufacier for technical assistance and to Diana Warwick for correcting the English text.

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Author notes

  1. Christophe Mougel

    Present address: INRA, UMR1349 IGEPP, 35653, Le Rheu, France

  2. Cécile Gubry-Rangin

    Present address: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, AB24 3UU, UK

Authors and Affiliations

  1. Agroécologie, AgroSup Dijon, CNRS, INRA, Université Bourgogne Franche-Comté, 21000, Dijon, France

    Amandine Viollet, Barbara Pivato, Christophe Mougel, Philippe Lemanceau & Sylvie Mazurier

  2. INRA, UMR 113 ‘Laboratoire des Symbioses Tropicales et Méditerranéennes’, Campus International de Baillarguet, TA-A82/J, 34398, Montpellier Cedex 5, France

    Jean-Claude Cleyet-Marel & Cécile Gubry-Rangin

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  1. Amandine Viollet
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  2. Barbara Pivato
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Correspondence to Sylvie Mazurier.

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Viollet, A., Pivato, B., Mougel, C. et al. Pseudomonas fluorescens C7R12 type III secretion system impacts mycorrhization of Medicago truncatula and associated microbial communities. Mycorrhiza 27, 23–33 (2017). https://doi.org/10.1007/s00572-016-0730-3

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