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TonB-dependent outer-membrane proteins and siderophore utilization in Pseudomonas fluorescens Pf-5

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Abstract

The soil bacterium Pseudomonas fluorescens Pf-5 produces two siderophores, a pyoverdine and enantio-pyochelin, and its proteome includes 45 TonB-dependent outer-membrane proteins, which commonly function in uptake of siderophores and other substrates from the environment. The 45 proteins share the conserved β-barrel and plug domains of TonB-dependent proteins but only 18 of them have an N-terminal signaling domain characteristic of TonB-dependent transducers (TBDTs), which participate in cell-surface signaling systems. Phylogenetic analyses of the 18 TBDTs and 27 TonB-dependent receptors (TBDRs), which lack the N-terminal signaling domain, suggest a complex evolutionary history including horizontal transfer among different microbial lineages. Putative functions were assigned to certain TBDRs and TBDTs in clades including well-characterized orthologs from other Pseudomonas spp. A mutant of Pf-5 with deletions in pyoverdine and enantio-pyochelin biosynthesis genes was constructed and characterized for iron-limited growth and utilization of a spectrum of siderophores. The mutant could utilize as iron sources a large number of pyoverdines with diverse structures as well as ferric citrate, heme, and the siderophores ferrichrome, ferrioxamine B, enterobactin, and aerobactin. The diversity and complexity of the TBDTs and TBDRs with roles in iron uptake clearly indicate the importance of iron in the fitness and survival of Pf-5 in the environment.

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Acknowledgments

We gratefully acknowledge the contributions of Dimitri Mavrodi in making the pchC mutant of Pf-5, and Harald Gross, Marcella Henkels and Kedy Shen in characterizing the role of orfamide A in the CAS agar assays. We thank Jeff Chang, Martin Schuster, Mark Silby, Johan Leveau and Gail Preston for providing cultures, and Cornelia Reimmann for the gift of authentic enantio-pyochelin. We are also grateful to Steven Giovannoni for advice on phylogenetic analyses, Philip Bronstein for advice on arbitrary PCR, and Jeff Chang and Martin Schuster for reviewing the manuscript. This research was supported by National Research Initiative Competitive Grants 2006-35319-17427 and 2008-35600-18770 from the USDA Cooperative State Research, Education, and Extension Service. We also gratefully acknowledge a fellowship to MCQ from the State of São Paulo Research Foundation (FAPESP), Brazil.

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  1. Department of Botany and Plant Pathology, Oregon State University, 2082 Cordley Hall, Corvallis, OR, 97331, USA

    Sierra L. Hartney

  2. INRA, Université de Bourgogne, UMR1229 ‘Microbiologie du Sol et de l’Environement’, CMSE, BV 86510, 21034, Dijon Cedex, France

    Sylvie Mazurier & Philippe Lemanceau

  3. Department of Genetics, Escola Superior de Agricultura ‘‘Luiz de Queiroz’’, University of São Paulo, 11 Pádua Dias Avenue, Piracicaba, SP, Brazil

    Maria Carolina Quecine

  4. Horticultural Crops Research Laboratory, United States Department of Agriculture, Agricultural Research Service, 3420 N.W. Orchard Avenue, Corvallis, OR, 97330, USA

    Teresa A. Kidarsa & Joyce E. Loper

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Hartney, S.L., Mazurier, S., Kidarsa, T.A. et al. TonB-dependent outer-membrane proteins and siderophore utilization in Pseudomonas fluorescens Pf-5. Biometals 24, 193–213 (2011). https://doi.org/10.1007/s10534-010-9385-2

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