Metabolomics of tomato xylem sap during bacterial wilt reveals <i>Ralstonia solanacearum</i> produces abundant putrescine, a metabolite that accelerates wilt disease

Lowe‐Power, Tiffany M.; Hendrich, Connor G.; Roepenack‐Lahaye, Edda von; Li, Bin; Wu, Dousheng; Mitra, Raka M.; Dalsing, Beth L.; Ricca, Patrizia; Naidoo, Jacinth; Cook, David E.; Jancewicz, Amy L.; Masson, Patrick; Thomma, B.P.H.J.; Lahaye, Thomas; Michael, Anthony J.; Allen, Caitilyn

doi:10.1111/1462-2920.14020

Cited by 116 publications

(139 citation statements)

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“…Typhimurium (Green et al, 2011). Putrescine is essential for growth of β-proteobacterium Ralstonia solanacearum (Lowe-Power et al, 2018). The spirochaete and agent of Lyme Disease Borrelia burgdorferi does not synthesize polyamines but it is absolutely dependent on the spermidine uptake transporter potABCD for growth (Bontemps-Gallo et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Polyamine‐independent growth and biofilm formation, and functional spermidine/spermine N‐acetyltransferases in Staphylococcus aureus and Enterococcus faecalis

Maezato

Kim

et al. 2018

Molecular Microbiology

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Summary Polyamines such as spermidine and spermine are primordial polycations that are ubiquitously present in the three domains of life. We have found that Gram‐positive bacteria Staphylococcus aureus and Enterococcus faecalis have lost either all or most polyamine biosynthetic genes, respectively, and are devoid of any polyamine when grown in polyamine‐free media. In contrast to bacteria such as Pseudomonas aeruginosa, Campylobacter jejuni and Agrobacterium tumefaciens, which absolutely require polyamines for growth, S. aureus and E. faecalis grow normally over multiple subcultures in the absence of polyamines. Furthermore, S. aureus and E. faecalis form biofilms normally without polyamines, and exogenous polyamines do not stimulate growth or biofilm formation. High levels of external polyamines, including norspermidine, eventually inhibit biofilm formation through inhibition of planktonic growth. We show that spermidine/spermine N‐acetyltransferase (SSAT) homologues encoded by S. aureus USA300 and E. faecalis acetylate spermidine, spermine and norspermidine, that spermine is the more preferred substrate, and that E. faecalis SSAT is almost as efficient as human SSAT with spermine as substrate. The polyamine auxotrophy, polyamine‐independent growth and biofilm formation, and presence of functional polyamine N‐acetyltransferases in S. aureus and E. faecalis represent a new paradigm for bacterial polyamine biology.

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Section: Introductionmentioning

confidence: 99%

Polyamine‐independent growth and biofilm formation, and functional spermidine/spermine N‐acetyltransferases in Staphylococcus aureus and Enterococcus faecalis

Maezato

Kim

et al. 2018

Molecular Microbiology

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“…Genes coding for the respective enzymes to catalyze the reactions and metabolites are presented in abbreviated form. The abbreviations used are the following: G6P, glucose-6phosphate; F6P, fructose-6-phosphate; FBP, fructose 1,6-bisphosphate; G3P, glyceraldehyde 3-phosphate; DHAP, dihydroxyacetone phosphate; G-1,5-6P, glucono-1-5-lactone-6-phosphate; 6PG, phosphogluconate; KDPG, 2-keto-3-deoxy-6-phosphogluconate; Ru5P, ribulose 5-phosphate; R5P, ribose 5 (Table S1). Experimental evidence in relation to the absence of these pathways in R. solanacearum was generated by parallel feeding of multiple [ 13 C]glucose substrates and tracking the label redistribution.…”

Section: Resultsmentioning

confidence: 99%

The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

et al. 2020

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In Ralstonia solanacearum, a devastating phytopathogen whose metabolism is poorly understood, we observed that the Entner-Doudoroff (ED) pathway and nonoxidative pentose phosphate pathway (non-OxPPP) bypass glycolysis and OxPPP under glucose oxidation. Evidence derived from 13 C stable isotope feeding and genome annotation-based comparative metabolic network analysis supported the observations. Comparative metabolic network analysis derived from the currently available 53 annotated R. solanacearum strains, including a recently reported strain (F1C1), representing the four phylotypes, confirmed the lack of key genes coding for phosphofructokinase (pfk-1) and phosphogluconate dehydrogenase (gnd) enzymes that are relevant for glycolysis and OxPPP, respectively. R. solanacearum F1C1 cells fed with [ 13 C]glucose (99% [1-13 C]glucose or 99% [1,2-13 C]glucose or 40% [ 13 C 6 ]glucose) followed by gas chromatography-mass spectrometry (GC-MS)-based labeling analysis of fragments from amino acids, glycerol, and ribose provided clear evidence that rather than glycolysis and the OxPPP, the ED pathway and non-OxPPP are the main routes sustaining metabolism in R. solanacearum. The 13 C incorporation in the mass ions of alanine (m/z 260 and m/z 232), valine (m/z 288 and m/z 260), glycine (m/z 218), serine (m/z 390 and m/z 362), histidine (m/z 440 and m/z 412), tyrosine (m/z 466 and m/z 438), phenylalanine (m/z 336 and m/z 308), glycerol (m/z 377), and ribose (m/z 160) mapped the pathways supporting the observations. The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13 C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. IMPORTANCE Understanding the metabolic versatility of Ralstonia solanacearum is important, as it regulates the trade-off between virulence and metabolism (1, 2) in a wide range of plant hosts. Due to a lack of clear evidence until this work, several published research papers reported on the potential roles of glycolysis and the oxidative pentose phosphate pathway (OxPPP) in R. solanacearum (3,4). This work provided evidence from 13 C stable isotope feeding and genome annotation-based comparative metabolic network analysis that the Entner-Doudoroff pathway and non-OxPPP bypass glycolysis and OxPPP during the oxidation of glucose, a component of the host xylem pool that serves as a potential carbon source (5). The outcomes help better define the central carbon metabolic network of R. solanacearum that can be integrated with 13 C metabolic flux analysis as well as flux balance analysis studies for defining the metabolic phenotypes. The study highlights the need to critically examine phytopathogens whose metabolism is poorly understood. on July 10, 2020 by guest http://msystems.asm.org/ Downloaded from R alstonia solanacearum is one of the most destructive plant pathogens as it infects over 450 plant species (6-8), and its metabolism is poorly understood. It is a soilborne pathogen that enters plan...

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“…In contrast to the important but not critical role of polyamines in planktonic growth of E. coli, polyamine biosynthesis is absolutely essential for growth of opportunistic pathogen ␥-proteobacterium Pseudomonas aeruginosa PAO1 (62), foodborne pathogen ⑀-proteobacterium Campylobacter jejuni (63), plant pathogen ␣-proteobacterium Agrobacterium tumefaciens C58 (64), and plant pathogen ␤-proteobacterium Ralstonia solanacearum (65). Whereas P. aeruginosa, C. jejuni, and A. tumefaciens synthesize spermidine, R. solanacearum produces only putrescine and 2-hydroxyputrescine (66) (Fig.…”

Section: Roles In Cell Growthmentioning

confidence: 99%

Polyamine function in archaea and bacteria

Michael

2018

Journal of Biological Chemistry

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Most of the phylogenetic diversity of life is found in bacteria and archaea, and is reflected in the diverse metabolism and functions of bacterial and archaeal polyamines. The polyamine spermidine was probably present in the last universal common ancestor, and polyamines are known to be necessary for critical physiological functions in bacteria, such as growth, biofilm formation, and other surface behaviors, and production of natural products, such as siderophores. There is also phylogenetic diversity of function, indicated by the role of polyamines in planktonic growth of different species, ranging from absolutely essential to entirely dispensable. However, the cellular molecular mechanisms responsible for polyamine function in bacterial growth are almost entirely unknown. In contrast, the molecular mechanisms of essential polyamine functions in archaea are better understood: covalent modification by polyamines of translation factor aIF5A and the agmatine modification of tRNA Ile . As with bacterial hyperthermophiles, archaeal thermophiles require long-chain and branched polyamines for growth at high temperatures. For bacterial species in which polyamines are essential for growth, it is still unknown whether the molecular mechanisms underpinning polyamine function involve covalent or noncovalent interactions. Understanding the cellular molecular mechanisms of polyamine function in bacterial growth and physiology remains one of the great challenges for future polyamine research. Figure 4. Polyamine dependence of biofilm formation in B. subtilis. WT, B. subtilis NCIB3610; ⌬speA, deletion mutant of arginine decarboxylase; Spd, spermidine; Nspd, norspermidine. Complex colony biofilms were grown on solid MSgg medium. Adapted from Hobley et al. (86).

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Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Cited by 116 publications

References 81 publications

Polyamine‐independent growth and biofilm formation, and functional spermidine/spermine N‐acetyltransferases in Staphylococcus aureus and Enterococcus faecalis

Polyamine‐independent growth and biofilm formation, and functional spermidine/spermine N‐acetyltransferases in Staphylococcus aureus and Enterococcus faecalis

The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum

Polyamine function in archaea and bacteria

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