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The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacteriumspp. and Staphylococcus spp. with potential plant-growth promoting activities

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Abstract

Background and aims

Plant seeds are emerging micro–habitats, whose importance as reservoir and vector of beneficial microbes just begins to be recognized. Here we aimed to characterize the bacterial microbiota of the Anadenanthera colubrina seed endosphere, with special focus to beneficial traits and to the colonization pattern.

Methods

Cultivation–dependent (isolation from surface–sterilized seeds) and cultivation–independent (pyrosequencing of 16S rRNA gene from metagenomic seed DNA) analyses, functional tests and microscopical investigations (fluorescence in situ hybridization coupled with confocal laser scanning microscopy (FISH-CLSM) were performed.

Results

We isolated several Methylobacterium and Staphylococcus spp., exhibiting both plant growth promotion and antimicrobial activities. The two taxonomic groups showed complementary traits, which supports a functional selection. Both genera were detected also by pyrosequencing, together with further taxa. The genera Friedmaniella, Bifidobacterium, Delftia, Anaerococcus and Actinomyces appeared here for the first time as seed endophytes. We detected bacterial cells and micro–colonies in seed cryosections by FISH-CLSM. Alphaproteobacteria, Firmicutes and other bacteria colonized intercellular spaces of the parenchyma and associated to transport vessels.

Conclusions

This work sheds light onto the diversity, functions and colonization pattern of the Anadenanthera colubrina seed endophytes, and strongly suggest a role as beneficial partners for seed-associated microbiota.

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Acknowledgements

Rita Geissler-Plaum (Giessen) is warmly acknowledged for the help in the laboratory and for her unlimited patience. We appreciate and acknowledge Karl–Heinz Kogel (Institute of Phytopatology, JLU-Giessen), for allowing M.C., P.A. and MD M.R. to use the confocal microscope. P.A. received a grant “Borse di perfezionamento studi all’estero” by the University of Palermo. This work was partially funded by Fondo Finalizzato alla Ricerca (FFR 2012- 2013) of the University of Palermo to A.M.P, and by CIUNSA (Consejo de Investigación de la universidad Nacional de Salta) to M.L.d.V.

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Author notes

  1. Carlotta De Filippo

    Present address: Institute of Agricultural Biology and Biotechnology – National Research Council (IBBA-CNR), Via Moruzzi 1, 56124, Pisa, Italy

Authors and Affiliations

  1. Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Viale delle Scienze ed.16, 90128, Palermo, Italy

    Pasquale Alibrandi, Paolo Ciná, Giuseppe Gallo & Anna Maria Puglia

  2. Institute of Applied Microbiology, Justus–Liebig–University Giessen, Heinrich–Buff–Ring 26–32, 35392, Giessen, Germany

    Massimiliano Cardinale, MD Mahafizur Rahman & Sylvia Schnell

  3. Computational Biology Research Unit, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010, San Michele all’ Adige, Italy

    Francesco Strati

  4. Banco de Germoplasma de Especies Nativas, Instituto de Ecología y Ambiente Humano, Universidad Nacional de Salta, UNSA, Av.da Bolivia 5150, 4400, Salta, Argentina

    Marta L. de Viana & Eugenia M. Giamminola

  5. Institute of Biometeorology – National Research Council (IBIMET-CNR), Via Caproni 8, 50145, Florence, Italy

    Carlotta De Filippo

  6. Istituto di Biomedicina e Immunologia Molecolare “A. Monroy” Consiglio Nazionale delle Ricerche CNR, Via La Malfa 153, 90146, Palermo, Italy

    Mirella Ciaccio

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  1. Pasquale Alibrandi
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Correspondence to Massimiliano Cardinale.

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Responsible Editor: Philippe Simoneau.

Massimiliano Cardinale is co–first author

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Alibrandi, P., Cardinale, M., Rahman, M.M. et al. The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacteriumspp. and Staphylococcus spp. with potential plant-growth promoting activities. Plant Soil 422, 81–99 (2018). https://doi.org/10.1007/s11104-017-3182-4

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