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Aromatic compounds degradation plays a role in colonization of Arabidopsis thaliana and Acacia caven by Cupriavidus pinatubonensis JMP134

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Abstract

Plant rhizosphere and internal tissues may constitute a relevant habitat for soil bacteria displaying high catabolic versatility towards xenobiotic aromatic compounds. Root exudates contain various molecules that are structurally related to aromatic xenobiotics and have been shown to stimulate bacterial degradation of aromatic pollutants in the rhizosphere. The ability to degrade specific aromatic components of root exudates could thus provide versatile catabolic bacteria with an advantage for rhizosphere colonization and growth. In this work, Cupriavidus pinatubonensis JMP134, a well-known aromatic compound degrader (including the herbicide 2,4-dichlorophenoxyacetate, 2,4-D), was shown to stably colonize Arabidopsis thaliana and Acacia caven plants both at the rhizoplane and endorhizosphere levels and to use root exudates as a sole carbon and energy source. No deleterious effects were detected on these colonized plants. When a toxic concentration of 2,4-D was applied to colonized A. caven, a marked resistance was induced in the plant, showing that strain JMP134 was both metabolically active and potentially beneficial to its host. The role for the β-ketoadipate aromatic degradation pathway during plant root colonization by C. pinatubonensis JMP134 was investigated by gene inactivation. A C. pinatubonensis mutant derivative strain displayed a reduced ability to catabolise root exudates isolated from either plant host. In this mutant strain, a lower competence in the rhizosphere of A. caven was also shown, both in gnotobiotic in vitro cultures and in plant/soil microcosms.

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Acknowledgments

This work was funded by the FONDECYT grants 3090051, 1070343, and 1110850, and the Millennium Nucleus on “Plant Functional Genomics” grant P/06-009-F. This study is also part of the research program FONDAP 1501-0001 funded by CONICYT to the Center for Advanced Studies in Ecology and Biodiversity, Program 7. Additional support from a CONICYT grant 79090016 is acknowledged. A.Z and R.D. are T.K, CONICYT—PhD fellows.

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The authors have declared no conflict of interest.

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Authors and Affiliations

  1. Facultad de Ingeniería y Ciencias, Universidad Adolfo Ibáñez, 7941169, Santiago, Chile

    Thomas Ledger, Ana Zúñiga, Paola Dasencich, Raúl Donoso & Bernardo González

  2. Millennium Nucleus on Plant Functional Genomics. Center for Advanced Studies in Ecology and Biodiversity, Pontificia Universidad Católica de Chile, Santiago, Chile

    Thomas Ledger, Ana Zúñiga, Tatiana Kraiser, Raúl Donoso, Danilo Pérez-Pantoja & Bernardo González

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  1. Thomas Ledger
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  2. Ana Zúñiga
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Correspondence to Bernardo González.

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Ledger, T., Zúñiga, A., Kraiser, T. et al. Aromatic compounds degradation plays a role in colonization of Arabidopsis thaliana and Acacia caven by Cupriavidus pinatubonensis JMP134. Antonie van Leeuwenhoek 101, 713–723 (2012). https://doi.org/10.1007/s10482-011-9685-8

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