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Indexing the Pseudomonas specialized metabolome enabled the discovery of poaeamide B and the bananamides

Nature Microbiology volume 2, Article number: 16197 (2017) Cite this article

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An Erratum to this article was published on 23 January 2017

Abstract

Pseudomonads are cosmopolitan microorganisms able to produce a wide array of specialized metabolites. These molecules allow Pseudomonas to scavenge nutrients, sense population density and enhance or inhibit growth of competing microorganisms. However, these valuable metabolites are typically characterized one-molecule–one-microbe at a time, instead of being inventoried in large numbers. To index and map the diversity of molecules detected from these organisms, 260 strains of ecologically diverse origins were subjected to mass-spectrometry-based molecular networking. Molecular networking not only enables dereplication of molecules, but also sheds light on their structural relationships. Moreover, it accelerates the discovery of new molecules. Here, by indexing the Pseudomonas specialized metabolome, we report the molecular-networking-based discovery of four molecules and their evolutionary relationships: a poaeamide analogue and a molecular subfamily of cyclic lipopeptides, bananamides 1, 2 and 3. Analysis of their biosynthetic gene cluster shows that it constitutes a distinct evolutionary branch of the Pseudomonas cyclic lipopeptides. Through analysis of an additional 370 extracts of wheat-associated Pseudomonas, we demonstrate how the detailed knowledge from our reference index can be efficiently propagated to annotate complex metabolomic data from other studies, akin to the way in which newly generated genomic information can be compared to data from public databases.

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Figure 1: Pseudomonas molecular network: environmental isolation visualization.
Figure 2: A molecular family comprising related peptides including viscosin, WLIP, viscosinamide, massetolides A–F, orfamides A–C and tensin.
Figure 3: MS/MS comparison of select molecules from the cyclic lipopeptide molecular family.
Figure 4: Evolutionary relationships between the assembly lines of the newly identified cyclic lipopeptides and structurally related molecules, based on their constituent phylogenetic groups of adenylation domains (Supplementary Fig. 12).
Figure 5: The cyclic lipopeptide molecular family upon addition of the 370 wheat-associated samples from the UK.

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Acknowledgements

Financial support was provided by the National Institutes of Health (NIH) grant GM097509 (to B.S.M. and P.C.D.). M.H.M. was supported by Rubicon (825.13.001) and Veni (863.15.002) grants from the Netherlands Organization for Scientific Research (NWO). J.R. and V.J.C. were supported by a grant from the Netherlands BEBasic Foundation (project F07.003.01) R.D.M. was supported by KU Leuven grant GOA/011/2008. M.G.K.G. is the recipient of a post-doctoral fellowship from FWO Vlaanderen (12M4615N). A.M.K. and T.L.C. were supported by NSF grants DEB-1115895 and DEB-1336290 and US FWS grant F12AP01081. L.M.S. was supported by a National Institutes of Health IRACDA K12 GM068524 grant award. J.G.M. was supported by BBSRC Institute Strategic Program (ISPG) grant BB/J004553/1 and University of East Anglia start-up funding. T.H.M. was supported by the BBSRC Institute Strategic Program (ISPG) ‘Optimization of nutrients in soil-plant systems’ (BBS/E/C/00005196). The authors acknowledge Bruker and NIH grants GMS10RR029121 and P41-GM103484 for support in the form of shared instrumentation and the computational infrastructure. NMR data were acquired at the University of California, San Diego Skaggs School of Pharmacy and Pharmaceutical Sciences NMR Facility. The authors thank V.V. Phelan for a review of this manuscript and M. Wang, A.T. Nelson and L.-F. Nothias-Scaglia for contributions.

Author information

Author notes

  1. Don D. Nguyen and Alexey V. Melnik: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of California San Diego, California, 92093, USA

    Don D. Nguyen & Jinshu Fang

  2. Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, California, 92093, USA

    Alexey V. Melnik, Nobuhiro Koyama & Pieter C. Dorrestein

  3. Graduate School of Pharmaceutical Sciences, Kitasato University, Tokyo, 108-8641, Japan

    Nobuhiro Koyama

  4. Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands

    Xiaowen Lu & Marnix H. Medema

  5. Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, California, 92093, USA

    Michelle Schorn, Bradley S. Moore & Pieter C. Dorrestein

  6. Ion Torrent by Thermo Fisher, 5781 Van Allen Way, Carlsbad, 92008, California, USA

    Kristen Aguinaldo & Tommie L. Lincecum Jr

  7. Centre of Microbial and Plant Genetics, KU Leuven, 3001 Heverlee, Belgium

    Maarten G. K. Ghequire & René De Mot

  8. Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6708PB Wageningen, The Netherlands

    Victor J. Carrion & Jos M. Raaijmakers

  9. Department of Ecology and Evolutionary Biology, University of California, 1156 High Street, Santa Cruz, 95064, California, USA

    Tina L. Cheng & A. Marm Kilpatrick

  10. Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, California, 92093, USA

    Brendan M. Duggan, Laura M. Sanchez, Bradley S. Moore & Pieter C. Dorrestein

  11. Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

    Jacob G. Malone

  12. School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

    Jacob G. Malone

  13. Department of AgroEcology, Rothamsted Research, West Common, Harpenden, AL5 2JQ, UK

    Tim H. Mauchline

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  1. Don D. Nguyen
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Contributions

D.D.N., A.V.M., X.L., M.H.M. and P.C.D. designed the research. D.D.N., A.V.M., N.K., X.L., M.S., J.F., K.A., T.L.L., B.M.D., B.S.M., M.H.M. and P.C.D. performed research. D.D.N., A.V.M., N.K., X.L., M.S., M.G.K.G., J.F., B.M.D., R.D.M., M.H.M. and P.C.D. analysed data. M.G.K.G., V.J.C., T.L.C., J.G.M., T.H.M., L.M.S., A.M.K., J.M.R. and R.D.M. contributed microbial strains or extracts. D.D.N., A.V.M. and P.C.D. wrote the paper.

Corresponding authors

Correspondence to Marnix H. Medema or Pieter C. Dorrestein.

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Supplementary information

Supplementary information

Legends for Supplementary Tables 1–8, Supplementary Figures 1–16 (PDF 4360 kb)

Supplementary Table 1

Known Pseudomonas specialized metabolites versus strain collection. A list of the 260 Pseudomonas isolates and the additional 370 wheat-associated samples from the UK, their collection information (if available), and the known compounds they contribute to. (XLSX 144 kb)

Supplementary Table 2

Known Pseudomonas specialized metabolites molecular families versus strain collection. A list of the 260 Pseudomonas isolates and the additional 370 wheat- associated samples from the UK, their collection information (if available), and the molecular families they contribute to. (XLSX 156 kb)

Supplementary Table 3

A summary table of known Pseudomonas specialized metabolites observed and the number of strains that contribute to them. (XLSX 17 kb)

Supplementary Table 4

A summary table of known Pseudomonas specialized metabolite molecular families that were observed and the number of strains that contribute to them. (XLSX 23 kb)

Supplementary Table 5

Supplementary Table 5. Poaeamide B (m/z 1,253) NMR table. MS/MS provided the amino acid sequence tag. Amino acid, 3-hydroxy acyl chain chemical shifts and measured coupling constants obtained from 2D 1H-13C heteronuclear single quantum coherence (HSQC), 2D 1H-13C heteronuclear multiple bond correlation (HMBC), 2D 1H-13C double quantum filtered correlation spectroscopy (COSY), and 1H-NMR spectra were used to confirm the identity of the amino acid residues and 3-hydroxy acyl chain specification. (XLSX 14 kb)

Supplementary Table 6

Bananamide 1, 2, and 3 NMR table. MS/MS provided the amino acid sequence tag. Amino acid, 3-hydroxy acyl chain chemical shifts and measured coupling constants obtained from 2D 1H-13C heteronuclear single quantum coherence (HSQC), 2D 1H-13C heteronuclear multiple bond correlation (HMBC), 2D 1H-13C double quantum filtered correlation spectroscopy (DQF-COSY), and 1H-NMR spectra were used to confirm the identity of the amino acid residues and 3-hydroxy acyl chains specification. (XLSX 15 kb)

Supplementary Table 7

Poaeamide B gene cluster table. Genes in the poaeamide B biosynthetic gene cluster from P. synxantha CR32 based on homology and protein domain analysis. (XLSX 11 kb)

Supplementary Table 8

Bananamide gene cluster table. Genes in the bananamide biosynthetic gene cluster from P. fluorescens BW11P2 based on homology and protein domain analysis. (XLSX 10 kb)

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Nguyen, D., Melnik, A., Koyama, N. et al. Indexing the Pseudomonas specialized metabolome enabled the discovery of poaeamide B and the bananamides. Nat Microbiol 2, 16197 (2017). https://doi.org/10.1038/nmicrobiol.2016.197

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