Response of Xylella fastidiosa to zinc: Decreased culturability, increased exopolysaccharide production, and formation of resilient biofilms under flow conditions

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 1097-1107

  Navarrete, Fernando ^a   De La Fuente, Leonardo ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL COMPOSITIONS; DISEASE DEVELOPMENT; EXOPOLYSACCHARIDES; FLOW CULTURE CONDITIONS; MICROFLUIDIC CHAMBERS; PLEIOTROPIC EFFECTS; VIABLE BUT NON-CULTURABLE; XYLELLA FASTIDIOSA;

BACTERIA; BIOFILMS; LIQUIDS; METABOLITES; MINERALS;

ZINC;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; BIOLOGICAL PRODUCTION; CHEMICAL COMPOSITION; ECOSYSTEM RESILIENCE; EFFICIENCY MEASUREMENT; FLOW PATTERN; GROWTH RESPONSE; HOST PLANT; MICROBIAL ACTIVITY; PATHOGEN; PLEIOTROPY; POLYSACCHARIDE; VIABILITY; XYLEM; ZINC;

BACTERIAL POLYSACCHARIDE; ZINC;

ARTICLE; BIOFILM; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MICROFLUIDIC ANALYSIS; PHYSIOLOGY; XYLELLA;

BIOFILMS; MICROBIAL VIABILITY; MICROFLUIDIC ANALYTICAL TECHNIQUES; POLYSACCHARIDES, BACTERIAL; XYLELLA; ZINC;

EID: 84893025855     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02998-13     Document Type: Article

References (92)

1. Hopkins DL, Purcell AH. 2002. Xylella fastidiosa: cause of Pierce's disease of grapevine and other emergent diseases. Plant Dis. 86:1056-1066. http: //dx.doi.org/10.1094/PDIS.2002.86.10.1056.
2. Chatterjee S, Almeida RPP, Lindow S. 2008. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu. Rev. Phytopathol. 46:243-271. http://dx.doi.org/10.1146/annurev.phyto.45.062806.094342.
3. Chang CJ, Donaldson R, Brannen P, Krewer G, Boland R. 2009. Bacterial leaf scorch, a new blueberry disease caused by Xylella fastidiosa. Hort. Sci. 44:413-417.
4. Hopkins DL. 1989. Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annu. Rev. Phytopathol. 27:271-290. http://dx.doi.org/10.1146 /annurev.py.27.090189.001415.
5. Goodwin PH, Devay JE, Meredith CP. 1988. Physiological responses of Vitis vinifera cv. Chardonnay to infection by the Pierce's disease bacterium. Physiol. Mol. Plant Pathol. 32:17-32.
6. Choi HK, Goes da Silva LAF, Cook DR. 2013. Water deficit modulates the response of Vitis vinifera to the Pierce's disease pathogen Xylella fastidiosa. Mol. Plant Microbe Interact. 26:643-657. http://dx.doi.org/10.1094/MPMI-09-12-0217-R.
7. De La Fuente L, Parker JK, Oliver JE, Granger S, Brannen PM, van Santen E, Cobine PA. 2013. The bacterial pathogen Xylella fastidiosa affects the leaf ionome of plant hosts during infection. PLoS One 8:e62945. http://dx.doi.org/10.1371/journal.pone.0062945.
8. Andersen PC, French WJ. 1987. Biophysical characteristics of peach trees infected with phony peach disease. Physiol. Mol. Plant Pathol. 31:25-40. http://dx.doi.org/10.1016/0885-5765(87)90004-X.
9. Silva-Stenico ME, Pacheco FTH, Pereira ER, Rodrigues JLM, Souza AN, Etchegaray A, Gomes JE, Tsai SM. 2009. Nutritional deficiency in citrus with symptoms of citrus variegated chlorosis disease. Braz. J. Biol. 69:859- 864. http://dx.doi.org/10.1590/S1519-69842009000400013.
10. Queiroz-Voltan RB, Paradela Filho O, Carelli ML, Fahl JI. 1998. Aspectos estruturais de cafeteiro infectado com Xylella fastidiosa. Bragantia 57. http://dx.doi.org/10.1590/S0006-87051998000100003.
11. Malavolta E, Prates NS. 1991. Alteracoes na composicao mineral das folhas de pomares citricos afetados pela anomalia "amarelinho" ou clorose variegada. Laranja 12:315-329.
12. Cruz LF, Cobine PA, De La Fuente L. 2012. Calcium increases surface attachment, biofilm formation, and twitching motility in Xylella fastidiosa. Appl. Environ. Microbiol. 78:1321-1331. http://dx.doi.org/10.1128/AEM.06501-11.
13. Cobine PA, Cruz LF, Navarrete F, Duncan D, Tygart M, De La Fuente L. 2013. Xylella fastidiosa differentially accumulates mineral elements in biofilm and planktonic cells. PLoS One 8:e54936. http://dx.doi.org/10 .1371/journal.pone.0054936.
14. Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B. 2007. Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol. Lett. 274:210-217. http://dx.doi.org/10.1111/j.1574-6968.2007.00827.x.
15. Malavolta E, de Oliverira SC, Pereira C, Lavres J, Jr, Prates HS, Malavolta M, Ferreira M. 2005. Comoposicao mineral de folhas de citros afetadas por declinio, amarelinho (CVC), morte subita e Huanglongbing (HLB). Informacoes Agronomicas. http://swfrec.ifas.ufl.edu/hlb/database/pdf/22_Malavolta_05.pdf.
16. Brady J, Faske J, Faske T, McGahan D. 2010. Evaluating the impact of nutritional treatments on Xylella fastidiosa in grapevine. Phytopathology 100:S16.
17. Purcino RP, Medina CL, Martins D, Winck FV, Machado EC, Novello JC, Machado MA, Mazzafera P. 2007. Xylella fastidiosa disturbs nitrogen metabolism and causes a stress response in sweet orange Citrus sinensis cv. Pera. J. Exp. Bot. 58:2733-2744. http://dx.doi.org/10.1093/jxb/erm138.
18. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745. http: //dx.doi.org/10.1146/annurev.mi.49.100195.003431.
19. Branda SS, Vik S, Friedman L, Kolter R. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:20-26. http://dx.doi.org/10.1016/j.tim .2004.11.006.
20. Denny TP. 1995. Involvement of bacterial polysaccharides in plant pathogenesis. Annu. Rev. Phytopathol. 33:173-197. http://dx.doi.org/10.1146 /annurev.py.33.090195.001133.
21. Killiny N, Hernandez Martinez R, Dumenyo CK, Cooksey DA, Almeida RP. 2013. The exopolysaccharide of Xylella fastidiosa is essential for biofilm formation, plant virulence and vector transmission. Mol. Plant Microbe Interact. 26:1044-1053. http://dx.doi.org/10.1094/MPMI-09-12-0211-R.
22. Tang DJ, Li XJ, He YQ, Feng JX, Chen BS, Tang JL. 2005. The zinc uptake regulator zur is essential for the full virulence of Xanthomonas campestris pv. campestris. Mol. Plant Microbe Interact. 18:652-658. http: //dx.doi.org/10.1094/MPMI-18-0652.
23. Yang WF, Liu Y, Chen L, Gao TC, Hu BS, Zhang DF, Liu FQ. 2007. Zinc uptake regulator (zur) gene involved in zinc homeostasis and virulence of Xanthomonas oryzae pv. oryzae in rice. Curr. Microbiol. 54:307-314. http: //dx.doi.org/10.1007/s00284-006-0485-8.
24. Wells JM, Raju BC, Hung HY, Weisburg WG, Mandelco-Paul L, Brenner DJ. 1987. Xylella fastidiosa gen. nov., sp. nov: Gram-negative, xylem-limited, fastidious plant bacteria related to Xanthomonas spp. Int. J. Syst. Evol. Microbiol. 37:136-143. http://dx.doi.org/10.1099/00207713-37-2-136.
25. Newman KL, Almeida RPP, Purcell AH, Lindow SE. 2003. Use of a green fluorescent strain for analysis of Xyella fastidiosa colonization of Vitis vinifera. Appl. Environ. Microbiol. 69:7319-7327. http://dx.doi.org/10.1128/AEM.69.12.7319-7327.2003.
26. Davis MJ, Purcell AH, Thomson SV. 1980. Isolation media for the Pierce's disease bacterium. Phytopathology 70:425-429. http://dx.doi.org/10.1094/Phyto-70-425.
27. Davis MJ, French WJ, Schaad NW. 1981. Axenic culture of the bacteria associated with phony disease of peach and plum leaf scald. Curr. Microbiol. 6:309-314. http://dx.doi.org/10.1007/BF01566883.
28. Zaini PA, De La Fuente L, Hoch HC, Burr TJ. 2009. Grapevine xylem sap enhances biofilm development by Xylella fastidiosa. FEMS Microbiol. Lett. 295:129-134. http://dx.doi.org/10.1111/j.1574-6968.2009.01597.x.
29. Doyle J, Doyle JL. 1987. Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochem Bull. 19:11-15.
30. Nocker A, Camper AK. 2006. Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Appl. Environ. Microbiol. 72:1997-2004. http://dx.doi.org/10.1128/AEM.72.3.1997-2004.2006.
31. Francis M, Lin H, Cabrera-La Rosa J, Doddapaneni H, Civerolo EL. 2006. Genome-based PCR primers for specific and sensitive detection and quantification of Xylella fastidiosa. Eur. J. Plant Pathol. 115:203-213. http: //dx.doi.org/10.1007/s10658-006-9009-4.
32. De La Fuente L, Montanes E, Meng YZ, Li YX, Burr TJ, Hoch HC, Wu MM. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 73:2690-2696. http://dx.doi.org/10.1128/AEM.02649-06.
33. Barrere GC, Barber CE, Daniels MJ. 1986. Molecular cloning of genes involved in the production of the extracellular polysaccharide xanthan by Xanthomonas campestris pv. campestris. Int. J. Biol. Macromol. 8:372-374. http://dx.doi.org/10.1016/0141-8130(86)90058-9.
34. Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. 1951. A colorimetric method for the determination of sugars. Nature 168:167.
35. -δδCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
36. Chatterjee S, Killiny N, Almeida RPP, Lindow SE. 2010. Role of cyclic di-GMP in Xylella fastidiosa biofilm formation, plant virulence, and insect transmission. Mol. Plant Microbe Interact. 23:1356-1363. http://dx.doi.org/10.1094/MPMI-03-10-0057.
37. Chatterjee S, Wistrom C, Lindow SE. 2008. A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc. Natl. Acad. Sci. U. S. A. 105:2670-2675. http://dx.doi.org/10.1073/pnas.0712236105.
38. Clark ME, Edelmann RE, Duley ML, Wall JD, Fields MW. 2007. Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments. Environ Microbiol. 9:2844-2854. http://dx.doi.org/10.1111/j.1462-2920.2007.01398.x.
39. Wood PJ. 1980. Specificity in the interaction of direct dyes with polysaccharides. Carbohydr. Res. 85:271-287. http://dx.doi.org/10.1016/S0008-6215(00)84676-5.
40. Wood PJ, Fulcher RG, Stone BA. 1983. Studies on the specificity of interaction of cereal cell-wall components with Congo Red and Calcofluor- specific detection and histochemistry of (1-]3),(1-]4),-beta-Dglucan. J. Cereal Sci. 1:95-110. http://dx.doi.org/10.1016/S0733-5210(83)80027-7.
41. da Silva FR, Vettore AL, Kemper EL, Leite A, Arruda P. 2001. Fastidiangum: the Xylella fastidiosa exopolysaccharide possibly involved in bacterial pathogenicity. FEMS Microbiol. Lett. 203:165-171. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10836.x.
42. Andreini C, Banci L, Bertini I, Rosato A. 2006. Zinc through the three domains of life. J. Proteome Res. 5:3173-3178. http://dx.doi.org/10.1021/pr0603699.
43. Chvapil M. 1973. New aspects in the biological role of zinc: a stabilizer of macromolecules and biological membranes. Life Sci. 13:1041-1049. http: //dx.doi.org/10.1016/0024-3205(73)90372-X.
44. Blencowe DK, Morby AP. 2003. Zn(II) metabolism in prokaryotes. FEMS Microbiol. Rev. 27:291-311. http://dx.doi.org/10.1016/S0168-6445(03)00041-X.
45. McDevitt CA, Ogunniyi AD, Valkov E, Lawrence MC, Kobe B, McEwan AG, Paton JC. 2011. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7:e1002357. http://dx.doi.org/10.1371/journal.ppat.1002357.
46. Fones H, Preston GM. 2013. The impact of transition metals on bacterial plant disease. FEMS Microbiol. Rev. 37:495-519. http://dx.doi.org/10.1111/1574-6976.12004.
47. De La Fuente L, Navarrete F, Oliver JE, Cruz LF, Cobine PA. The influence of metal elements on virulence in plant pathogenic bacteria. In De La Fuente L, Wang N, Jones J, Ham J, White F, Sundin G, Hogenhaut S, Roper C (ed), Virulence mechanisms of plant pathogenic bacteria, in press. American Phytopathological Society Press, St. Paul, MN.
48. Ogasawara H, Shinohara S, Yamamoto K, Ishihama A. 2012. Novel regulation targets of the metal-response BasS-BasR two-component system of Escherichia coli. Microbiology 158:1482-1492. http://dx.doi.org/10.1099/mic.0.057745-0.
49. Datnoff LE, Elmer WH, Huber DM. 2007. Mineral nutrition and plant disease. American Phytopathological Society, St. Paul, MN.
50. Barker AV, Pilbeam DJ. 2007. Handbook of plant nutrition. CRC Press, Boca Raton, FL.
51. Wilcox W. 2013. Grape disease control, 2013, p 1-44. NY State Agricultural Experiment Station, Geneva, NY. http://www.fruit.cornell.edu/grape/pdfs/Wilcox-Grape%20Disease%20Control%202013.pdf.
52. Gubler WD, Smith RJ, Varela LG, Vasquez S, Stapleton JJ, Purcell AH. 2009.UCIPM pest management guidelines: grape-diseases, p 70-90. Publication 3448.UCStatewide IPM Program, University of California, Davis, CA. http://www.ipm.ucdavis.edu/PDF/PMG/pmggrape.pdf.
53. Marschner H. 1995. Mineral nutrition of higher plants, 2nd ed. Academic Press, San Diego, CA.
54. Roper MC, Greve LC, Labavitch JA, Kirkpatrick BC. 2007. Detection and visualization of an exopolysaccharide produced by Xylella fastidiosa in vitro and in planta. Appl. Environ. Microbiol. 73:7252-7258. http://dx.doi.org/10.1128/AEM.00895-07.
55. Killiny N, Almeida RPP. 2009. Host structural carbohydrate induces vector transmission of a bacterial plant pathogen. Proc. Natl. Acad. Sci. U. S. A. 106:22416-22420. http://dx.doi.org/10.1073/pnas.0908562106.
56. Wei CL, Lin NT, Weng SF, Tseng YH. 1996. The gene encoding UDPglucose pyrophosphorylase is required for the synthesis of xanthan gum in Xanthomonas campestris. Biochem. Biophys. Res. Commun. 226:607- 612. http://dx.doi.org/10.1006/bbrc.1996.1403.
57. Mollerach M, Lopez R, Garcia E. 1998. Characterization of the galU gene of Streptococcus pneumoniae encoding a uridine diphosphoglucose pyrophosphorylase: a gene essential for capsular polysaccharide biosynthesis. J. Exp. Med. 188:2047-2056. http://dx.doi.org/10.1084/jem.188.11.2047.
58. Sundararajan TA, Rapin AM, Kalckar HM. 1962. Biochemical observations on E. coli mutants defective in uridine diphosphoglucose. Proc. Natl. Acad. Sci. U. S. A. 48:2187-2193. http://dx.doi.org/10.1073/pnas.48.12.2187.
59. Bohin JP. 2000. Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol. Lett. 186:11-19. http://dx.doi.org/10.1016/S0378-1097(00)00110-5.
60. Breedveld MW, Miller KJ. 1994. Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol. Rev. 58:145-161.
61. Hotte B, Rath-Arnold I, Puhler A, Simon R. 1990. Cloning and analysis of a 35.3-kilobase DNA region involved in exopolysaccharide production by Xanthomonas campestris pv. campestris. J. Bacteriol. 172:2804-2807.
62. Koplin R, Arnold W, Hotte B, Simon R, Wang G, Puhler A. 1992. Genetics of xanthan production in Xanthomonas campestris: the xanA and xanB genes are involved in UDP-glucose and GDP-mannose biosynthesis. J. Bacteriol. 174:191-199.
63. Huang TP, Somers EB, Wong AC. 2006. Differential biofilm formation and motility associated with lipopolysaccharide/exopolysaccharidecoupled biosynthetic genes in Stenotrophomonas maltophilia. J. Bacteriol. 188:3116-3120. http://dx.doi.org/10.1128/JB.188.8.3116-3120.2006.
64. Whitchurch CB, Alm RA, Mattick JS. 1996. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 93:9839-9843. http: //dx.doi.org/10.1073/pnas.93.18.9839.
65. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700. http://dx.doi.org/10.1146/annurev.biochem.71.110601.135414.
66. Clifford JC, Rapicavoli JN, Roper MC. 2013. A rhamnose-rich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol. Plant Microbe Interact. 26:676- 685. http://dx.doi.org/10.1094/MPMI-12-12-0283-R.
67. Meng YZ, Li YX, Galvani CD, Hao GX, Turner JN, Burr TJ, Hoch HC. 2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560-5567. http://dx.doi.org/10.1128/JB.187.16.5560-5567.2005.
68. De La Fuente L, Burr TJ, Hoch HC. 2008. Autoaggregation of Xylella fastidiosa cells is influenced by type I and type IV pili. Appl. Environ. Microbiol. 74:5579-5582. http://dx.doi.org/10.1128/AEM.00995-08.
69. Sousa SA, Moreira LM, Leitao JH. 2008. Functional analysis of the Burkholderia cenocepacia J2315 BceAJ protein with phosphomannose isomerase and GDP-D-mannose pyrophosphorylase activities. Appl. Microbiol. Biotechnol. 80:1015-1022. http://dx.doi.org/10.1007/s00253-008-1612-1.
70. Vaara M. 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56:395-411.
71. Geddie JL, Sutherland IW. 1993. Uptake of metals by bacterial polysaccharides. J. Appl. Microbiol. 74:467-472. http://dx.doi.org/10.1111/j.1365-2672.1993.tb05155.x.
72. Wolfaardt G, Lawrence JR, Korber DR. 1999. Function of EPS, p 171- 200. In Wingender J, Neu TR, Flemming H-C (ed), Microbial extracellular polymeric substances. Springer, Berlin, Germany.
73. Bereswill S, Jock S, Bellemann P, Geider K. 1998. Identification of Erwinia amylovora by growth in the presence of copper sulfate and by capsule staining with lectin. Plant Dis. 82:158-164. http://dx.doi.org/10.1094/PDIS.1998.82.2.158.
74. Ordax M, Marco-Noales E, Lopez MM, Biosca EG. 2010. Exopolysaccharides favor the survival of Erwinia amylovora under copper stress through different strategies. Res. Microbiol. 161:549-555. http://dx.doi .org/10.1016/j.resmic.2010.05.003.
75. Oliver JD. 2000. The public health significance of viable but nonculturable bacteria, p 277-299. In Colwell RR, Grimes, DJ (ed), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
76. Oliver JD. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34:415-425. http://dx.doi.org /10.1111/j.1574-6976.2009.00200.x.
77. Oliver JD. 1995. The viable but non-culturable state in the human pathogen Vibrio vulnificus. FEMS Microbiol. Lett. 133:203-208. http://dx.doi .org/10.1111/j.1574-6968.1995.tb07885.x.
78. Alexander E, Pham D, Steck TR. 1999. The viable-but-nonculturable condition is induced by copper in Agrobacterium tumefaciens and Rhizobium leguminosarum. Appl. Environ. Microbiol. 65:3754-3756.
79. Grey B, Steck TR. 2001. Concentrations of copper thought to be toxic to Escherichia coli can induce the viable but nonculturable condition. Appl. Environ. Microbiol. 67:5325-5327. http://dx.doi.org/10.1128/AEM.67.11.5325-5327.2001.
80. Grey BE, Steck TR. 2001. The viable but nonculturable state of Ralstonia solanacearum may be involved in long-term survival and plant infection. Appl. Environ. Microbiol. 67:3866-3872. http://dx.doi.org/10.1128/AEM.67.9.3866-3872.2001.
81. Wilson M, Lindow SE. 2000. Viable but nonculturable cells in plantassociated bacterial populations, p 229-241. In Colwell RR, Grimes DJ (ed), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
82. del Campo R, Russi P, Mara P, Mara H, Peyrou M, de Leon IP, Gaggero C. 2009. Xanthomonas axonopodis pv. citri enters the VBNC state after copper treatment and retains its virulence. FEMS Microbiol. Lett. 298: 143-148. http://dx.doi.org/10.1111/j.1574-6968.2009.01709.x.
83. Ordax M, Marco-Noales E, Lopez MM, Biosca EG. 2006. Survival strategy of Erwinia amylovora against copper: induction of the viable-but-nonculturable state. Appl. Environ. Microbiol. 72:3482-3488. http://dx.doi.org/10.1128/AEM.72.5.3482-3488.2006.
84. Lleo M, Bonato B, Tafi MC, Caburlotto G, Benedetti D, Canepari P. 2007. Adhesion to medical device materials and biofilm formation capability of some species of enterococci in different physiological states. FEMS Microbiol. Lett. 274:232-237. http://dx.doi.org/10.1111/j.1574-6968.2007.00836.x.
85. Chaiyanan S, Chaiyanan S, Huq A, Maugel T, Colwell RR. 2001. Viability of the nonculturable Vibrio cholerae O1 and O139. Syst. Appl. Microbiol. 24:331-341. http://dx.doi.org/10.1078/0723-2020-00032.
86. Rudi K, Moen B, Drømtorp SM, Holck AL. 2005. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl. Environ. Microbiol. 71:1018-1024. http: //dx.doi.org/10.1128/AEM.71.2.1018-1024.2005.
87. Boulos L, Prevost M, Barbeau B, Coallier J, Desjardins R. 1999. LIVE/DEAD BacLight: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37:77-86. http://dx.doi.org/10.1016/S0167-7012(99)00048-2.
88. Mesa MM, Macias M, Cantero D, Barja F. 2003. Use of the direct epifluorescent filter technique for the enumeration of viable and total acetic acid bacteria from vinegar fermentation. J. Fluoresc. 13:261-265. http://dx.doi.org/10.1023/A:1025094017265.
89. Flekna G, Stefanic P, Wagner M, Smulders FJ, Mozina SS, Hein I. 2007. Insufficient differentiation of live and dead Campylobacter jejuni and Listeria monocytogenes cells by ethidium monoazide (EMA) compromises EMA/real-time PCR. Res. Microbiol. 158:405-412. http://dx.doi.org/10.1016/j.resmic.2007.02.008.
90. Newman KL, Almeida RPP, Purcell AH, Lindow SE. 2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc. Natl. Acad. Sci. U. S. A. 101:1737-1742. http://dx.doi.org/10.1073/pnas.0308399100.
91. Zaini PA, Fogaca AC, Lupo FGN, Nakaya HI, Vencio RZN, da Silva AM. 2008. The iron stimulon of Xylella fastidiosa includes genes for type IV pilus and colicin V-like bacteriocins. J. Bacteriol. 190:2368-2378. http: //dx.doi.org/10.1128/JB.01495-07.
92. Choi HK, Goes da Silva F, Lim HJ, Iandolino A, Seo YS, Lee SW, Cook DR. 2010. Diagnosis of Pierce's disease using biomarkers specific to Xylella fastidiosa rRNA and Vitis vinifera gene expression. Phytopathology 100:1089-1099. http://dx.doi.org/10.1094/PHYTO-01-10-0014. Xylella fastidiosa Response to Zinc