A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum

PLoS Pathogens

Volumn 12, Issue 10, 2016, Pages

  Peyraud, Rémi ^a   Cottret, Ludovic ^a   Marmiesse, Lucas ^a   Gouzy, Jérôme ^a   Genin, Stéphane ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; EXOPOLYSACCHARIDE; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; MICROARRAY ANALYSIS; MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHENOTYPE; PREDICTION; PROTEIN ANALYSIS; RALSTONIA SOLANACEARUM; RESOURCE ALLOCATION; VALIDATION STUDY; GRAM NEGATIVE INFECTION; METABOLISM; MICROBIOLOGY; NUCLEAR MAGNETIC RESONANCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; VIRULENCE;

CELL PROLIFERATION; GRAM-NEGATIVE BACTERIAL INFECTIONS; METABOLIC NETWORKS AND PATHWAYS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PLANT DISEASES; RALSTONIA SOLANACEARUM; VIRULENCE; VIRULENCE FACTORS;

EID: 84992755822     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005939     Document Type: Article

References (74)

1. Brown SA, Palmer KL, Whiteley M, Revisiting the host as a growth medium. Nat. Rev. Microbiol. 2008; 6:657–666. doi: 10.1038/nrmicro195518679171
2. Eisenreich W, Dandekar T, Heesemann J, Goebel W, Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat. Rev. Microbiol. 2010; 8:401–412. doi: 10.1038/nrmicro235120453875
3. Barbier T, Nicolas C, Letesson JJ, Brucella adaptation and survival at the crossroad of metabolism and virulence. FEBS Lett. 2011; 585:2929–2934. doi: 10.1016/j.febslet.2011.08.01121864534
4. Rohmer L, Hocquet D, Miller SI, Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 2011; 19:341–348. doi: 10.1016/j.tim.2011.04.00321600774
5. Schoen C, Kischkies L, Elias J, Ampattu BJ, Metabolism and virulence in Neisseria meningitidis. Front Cell Infect Microbiol. 2014; 4:114. doi: 10.3389/fcimb.2014.0011425191646
6. Rico A, Preston GM, Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact. 2008; 21:269–282. doi: 10.1094/MPMI-21-2-026918184070
7. Zhang YJ, Rubin EJ, Feast or famine: the host-pathogen battle over amino acids. Cell Microbiol. 2013; 15:1079–1087. doi: 10.1111/cmi.1214023521858
8. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature2010; 468:527–532. doi: 10.1038/nature0960621107422
9. Platt TG, Morton ER, Barton IS, Bever JD, Fuqua C, Ecological dynamics and complex interactions of Agrobacterium megaplasmids. Front Plant Sci. 2014; 5:635. doi: 10.3389/fpls.2014.0063525452760
10. Fatima U, Senthil-Kumar M, Plant and pathogen nutrient acquisition strategies. Front Plant Sci. 2015; 6:750. doi: 10.3389/fpls.2015.0075026442063
11. Abu Kwaik Y, Bumann D, Microbial quest for food in vivo: “nutritional virulence” as an emerging paradigm. Cell Microbiol. 2013; 15:882–890. doi: 10.1111/cmi.1213823490329
12. Ding Y, Liu X, Chen F, Di H, Xu B, Zhou L, et al. Metabolic sensor governing bacterial virulence in Staphylococcus aureus. Proc Natl Acad Sci USA. 2014; 111:E4981–E4990. doi: 10.1073/pnas.141107711125368190
13. Asrat S, Davis KM, Isberg RR, Modulation of the host innate immune and inflammatory response by translocated bacterial proteins. Cell Microbiol. 2015; 17:785–795. doi: 10.1111/cmi.1244525850689
14. Macho AP, Zipfel C, Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 2015; 23:14–22. doi: 10.1016/j.mib.2014.10.00925461568
15. Price CT, Al-Quadan T, Santic M, Rosenshine I, Abu Kwaik Y, Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science2011; 334: 1553–1557. doi: 10.1126/science.121286822096100
16. Baruch M, Hertzog BB, Ravins M, Youting CC, Hanski E, Group A streptococcus and host metabolism: virulence influences and potential treatments. Future Microbiol. 2014; 9:713–716. doi: 10.2217/fmb.14.3925046517
17. Vakulskas CA, Potts AH, Babitzke P, Ahmer BM, Romeo T, Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev. 2015;79:193–224. doi: 10.1128/MMBR.00052-1425833324
18. Ferenci T, Trade-off mechanisms shaping the diversity of bacteria. Trends Microbiol. 2016; 24:209–223. doi: 10.1016/j.tim.2015.11.00926705697
19. Maharjan R, Nilsson S, Sung J, Haynes K, Beardmore RE, Hurst LD, Ferenci T, Gudelj I, The form of a trade-off determines the response to competition. Ecol Lett. 2013; 16:1267–76. doi: 10.1111/ele.1215923902419
20. Molenaar D, van Berlo R, de Ridder D, Teusink B, Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol. 2009; 5:323. doi: 10.1038/msb.2009.8219888218
21. Peebo K, Valgepea K, Maser A, Nahku R, Adamberg K, Vilu R, Proteome reallocation in Escherichia coli with increasing specific growth rate. Mol Biosyst. 2015;11:1184–1193. doi: 10.1039/c4mb00721b25712329
22. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 2012; 13:614–629. doi: 10.1111/j.1364-3703.2012.00804.x22672649
23. Turner M, Jauneau A, Genin S, Tavella MJ, Vailleau F, Gentzbittel L, et al. Dissection of bacterial wilt on Medicago truncatula revealed two type III secretion system effectors acting on root infection process and disease development. Plant Physiol. 2009; 1501713–1722. doi: 10.1104/pp.109.14152319493968
24. Digonnet C, Martinez Y, Denancé N, Chasseray M, Dabos P, Ranocha P, et al. Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall. Planta. 2012; 236:1419–1431. doi: 10.1007/s00425-012-1694-y22729825
25. Genin S, Denny TP, Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol. 2012; 50:67–89. doi: 10.1146/annurev-phyto-081211-17300022559068
26. Jacobs JM, Babujee L, Meng F, Milling A, Allen C, The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. mBio. 2012; 3(4). pii: e00114–12. doi: 10.1128/mBio.00114-1222807564
27. Monteiro F, Genin S, van Dijk I, Valls M, A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection. Microbiology2012; 158:2107–2116. doi: 10.1099/mic.0.058610-022609750
28. McCloskey D, Palsson BØ, Feist AM, Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli. Mol Syst Biol. 2013; 9:661. doi: 10.1038/msb.2013.1823632383
29. Bordbar A, Monk JM, King ZA, Palsson BO, Constraint-based models predict metabolic and associated cellular functions. Nat Rev Genet. 2014; 15:107–120. doi: 10.1038/nrg364324430943
30. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, et al. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature2002; 415:497–502. doi: 10.1038/415497a11823852
31. Thiele I, Palsson BØ, A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat. Protoc. 2010; 5:93–121. doi: 10.1038/nprot.2009.20320057383
32. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, et al. A comprehensive genome-scale reconstruction of Escherichia coli metabolism—2011. Mol Syst Biol. 2011; 7:535. doi: 10.1038/msb.2011.6521988831
33. McGarvey JA, Denny TP, Schell MA, Spatial-temporal and quantitative analysis of growth and EPS I production by Ralstonia solanacearum in resistant and susceptible tomato cultivars. Phytopathology. 1999; 89:1233–1239. doi: 10.1094/PHYTO.1999.89.12.123318944650
34. Huang J, Yindeeyoungyeon W, Garg RP, Denny TP, Schell MA, Joint transcriptional control of xpsR, the unusual signal integrator of the Ralstonia solanacearum virulence gene regulatory network, by a response regulator and a LysR-type transcriptional activator. J Bacteriol. 1998;180:2736–2743. 9573161
35. Flavier AB, Clough SJ, Schell MA, Denny TP, Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol Microbiol. 1997; 26:251–259. 9383151
36. Zuluaga AP, Puigvert M, Valls M, Novel plant inputs influencing Ralstonia solanacearum during infection. Front. Microbiol. 2013; 4:349. doi: 10.3389/fmicb.2013.0034924312090
37. Valls M, Genin S, Boucher C, Integrated regulation of the Type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog. 2006; 2(8):e82. doi: 10.1371/journal.ppat.002008216933989
38. Oh Y-K, Palsson BO, Park SM, Schilling CH, Mahadevan R, Genome-scale reconstruction of metabolic network in Bacillus subtilis based on high-throughput phenotyping and gene essentiality data. J Biol Chem. 2007; 282:28791–28799. doi: 10.1074/jbc.M70375920017573341
39. Oberhardt MA, Puchałka J, Martins dos Santos VAP, Papin JA, Reconciliation of genome-scale metabolic reconstructions for comparative systems analysis. PLoS Comput Biol. 2011; 7(3):e1001116. doi: 10.1371/journal.pcbi.100111621483480
40. Peeters N, Carrère S, Anisimova M, Plener L, Cazalé AC, Genin S, Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex. BMC Genomics2013; 14:859. doi: 10.1186/1471-2164-14-85924314259
41. Lonjon F, Turner M, Henry C, Rengel D, Lohou D, van de Kerkhove Q, et al. Comparative secretome analysis of Ralstonia solanacearum Type 3 secretion-associated mutants reveals a fine control of effector delivery, essential for bacterial pathogenicity. Mol Cell Proteomics. 2016; 15:598–613. doi: 10.1074/mcp.M115.05107826637540
42. Vial L, Chapalain A, Groleau MC, Déziel E, The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol. 2011; 13:1–12. doi: 10.1111/j.1462-2920.2010.02343.x20880095
43. Guieysse B, Wuertz S, Metabolically versatile large-genome prokaryotes. Curr Opin Biotechnol. 2012; 23:467–473. doi: 10.1016/j.copbio.2011.12.02222226959
44. Guidot A, Prior P, Schoenfeld J, Carrère S, Genin S, Boucher C, Genomic structure and phylogeny of the plant pathogen Ralstonia solanacearum inferred from gene distribution analysis. J Bacteriol. 2007; 189:377–387. doi: 10.1128/JB.00999-0617085551
45. Remenant B, de Cambiaire J-C, Cellier G, Jacobs JM, Mangenot S, Barbe V, et al. Ralstonia syzygii, the Blood Disease Bacterium and some Asian R. solanacearum strains form a single genomic species despite divergent lifestyles. PloS One2011; 6(9):e24356. doi: 10.1371/journal.pone.002435621931687
46. Pérez-Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, et al. Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol. 2012; 14:1091–1117. doi: 10.1111/j.1462-2920.2011.02613.x22026719
47. Brumbley SM, Denny TP, Cloning of wild-type Pseudomonas solanacearum phcA, a gene that when mutated alters expression of multiple traits that contribute to virulence. J Bacteriol. 1990; 172:5677–5685. 2211505
48. Brumbley SM, Carney BF, Denny TP, Phenotype conversion in Pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional regulator. J Bacteriol. 1993; 175:5477–5487. 8366033
49. Gama JA, Abby SS, Vieira-Silva S, Dionisio F, Rocha EP, Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens. PLoS Pathog. 2012; 8(2):e1002503. doi: 10.1371/journal.ppat.100250322319444
50. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt WD, Doebeli M, Self-destructive cooperation mediated by phenotypic noise. Nature2008; 454:987–990. doi: 10.1038/nature0706718719588
51. Diard M, Garcia V, Maier L, Remus-Emsermann MNP, Regoes RR, Ackermann M, et al. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature2013; 494:353–356. doi: 10.1038/nature1191323426324
52. Winzer K, Williams P, Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int J Med Microbiol. 2001; 291:131–143. doi: 10.1078/1438-4221-0011011437336
53. Wei Z, Yang T, Friman VP, Xu Y, Shen Q, Jousset A, Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015; 6:8413. doi: 10.1038/ncomms941326400552
54. Kelman A, The relationship of pathogenicity of Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology1954; 44:693–695.
55. Poussier S, Thoquet P, Trigalet-Demery D, Barthet S, Meyer D, Arlat M, et al. Host plant-dependent phenotypic reversion of Ralstonia solanacearum from non-pathogenic to pathogenic forms via alterations in the phcA gene. Mol Microbiol. 2003; 49:991–1003. doi: 10.1046/j.1365-2958.2003.03605.x12890023
56. Guidot A, Jiang W, Ferdy J-B, Thébaud C, Barberis P, Gouzy J, et al. Multihost experimental evolution of the pathogen Ralstonia solanacearum unveils genes involved in adaptation to plants. Mol. Biol. Evol. 2014; 31:2913–2928. doi: 10.1093/molbev/msu22925086002
57. Genin S, Gough CL, Zischek C, Boucher CA, Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol. Microbiol. 1992; 6:3065–3076. doi: 10.1111/j.1365-2958.1992.tb01764.x1479894
58. Genin S, Brito B, Denny TP, Boucher C, Control of the Ralstonia solanacearum Type III secretion system (Hrp) genes by the global virulence regulator PhcA. FEBS Lett. 2005; 579:2077–2081. doi: 10.1016/j.febslet.2005.02.05815811321
59. Prentki P, Krisch HM, In vitro insertional mutagenesis with a selectable DNA fragment. Gene1984; 29:303–313. doi: 10.1016/0378-1119(84)90059-36237955
60. Plener L, Manfredi P, Valls M, Genin S, PrhG, a transcriptional regulator responding to growth conditions, is involved in the control of the Type III secretion system regulon in Ralstonia solanacearum. J Bacteriol. 2010; 192:1011–1019. doi: 10.1128/JB.01189-0920008073
61. Vaas LA, Sikorski J, Hofner B, Fiebig A, Buddruhs N, Klenk H-P, et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics2013; 29:1823–1824. doi: 10.1093/bioinformatics/btt29123740744
62. Park JM, Kim TY, Lee SY, Genome-scale reconstruction and in silico analysis of the Ralstonia eutropha H16 for polyhydroxyalkanoate synthesis, lithoautotrophic growth, and 2-methyl citric acid production. BMC Syst Biol. 2011; 5:101. doi: 10.1186/1752-0509-5-10121711532
63. Notebaart RA, van Enckevort FHJ, Francke C, Siezen RJ, Teusink B, Accelerating the reconstruction of genome-scale metabolic networks. BMC Bioinformatics2006; 7:296. doi: 10.1186/1471-2105-7-29616772023
64. Remm M, Storm CE, Sonnhammer EL, Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 2001; 314:1041–1052. doi: 10.1006/jmbi.2000.519711743721
65. Kanehisa M, Goto S, KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000; 28:27–30. doi: 10.1093/nar/28.1.2710592173
66. Caspi R, Altman T, Dreher K, Fulcher CA, Subhraveti P, Keseler IM, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2011; 40(D1):D742–D753. doi: 10.1093/nar/gkr101426527732
67. Saier MH, JrTran CV, Barabote RD, TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 2006; 34:D181–186. doi: 10.1093/nar/gkj00116381841
68. Karp PD, Paley S, Romero P, The Pathway Tools software. Bioinforma Oxf Engl. 2002; 18Suppl 1:S225–232. doi: 10.1093/bioinformatics/18.suppl_1.S22512169551
69. Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, et al. MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res. 2013; 41:D636–647. doi: 10.1093/nar/gks119423193269
70. Cottret L, Wildridge D, Vinson F, Barrett MP, Charles H, Sagot M-F, et al. MetExplore: a web server to link metabolomic experiments and genome-scale metabolic networks. Nucleic Acids Res. 2010; 38:W132–137. doi: 10.1093/nar/gkq31220444866
71. Courtot M, Juty N, Knüpfer C, Waltemath D, Zhukova A, Dräger A, et al. Controlled vocabularies and semantics in systems biology. Mol Syst Biol. 2011; 7:543. doi: 10.1038/msb.2011.7722027554
72. Peyraud R, Schneider K, Kiefer P, Massou S, Vorholt JA, Portais J-C, Genome-scale reconstruction and system level investigation of the metabolic network of Methylobacterium extorquens AM1. BMC Syst Biol. 2011; 5:189. doi: 10.1186/1752-0509-5-18922074569
73. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinforma Oxf Engl. 2010; 26:1608–1615. doi: 10.1093/bioinformatics/btq24920472543
74. Marmiesse L, Peyraud R, Cottret L, FlexFlux: combining metabolic flux and regulatory network analyses. BMC Syst. Biol. 2015; 9:93. doi: 10.1186/s12918-015-0238-z26666757