Bacillus mojavensis: Its Endophytic Nature, the Surfactins, and Their Role in the Plant Response to Infection by Fusarium verticillioides

Abstract

Bacterial endophytes are fundamentally important as natural components of most plants, wild and cultivated with strong ecological merits. These ancient associations are recently at the forefront of biological control strategies designed to circumvent the problems associated with pesticide uses, particularly on specific food crops. Bacterial endophytes form compatible associations that persist during the growing seasons, where several enhanced benefits are associated, suggesting that such associations are mutualistic. Several genera of bacteria are known as root associations, and only recently are species being identified as plant endophytes, occupying the entire plant axis in most cases. Bacillus mojavensis was discovered in maize kernels and later determined to be an endophyte with biocontrol potential due to its inhibition of the maize mycotoxic and pathogenic fungus Fusarium verticillioides, itself an endophyte. It was subsequently shown that this strain and others were inhibitory to most fungi, especially plant pathogenic species. Further, maize plants infected with B. mojavensis showed a marked improvement in foliage and root growth and development, disease protection, and mycotoxin reduction. Components of B. mojavensis-infected maize are reviewed relative to biocontrol of F. verticillioides and other endophytic fungi. The patented and other strains of this bacterium were recently reported as producers of the lipopeptide biosurfactant Leu7-surfactin. The chemistry, fermentation of the surfactins, and their uses, along with the essential features of surfactins required for fungal inhibition, are discussed. We also review the host–parasite relations of this bacterial endophyte, and its biochemical utility in an effort to bring attention to the potential qualities of B. mojavensis, and other bacterial endophytes for enhancers of plant growth and protectors of diseases.

References

  1. Abu-Ruwaida AS, Banat IM, Haditiro S, Salem A, Kadri M (1991) Isolation of biosurfactant – producing bacteria: product characterization and evaluation. Acta Biotechnol 10:315–324CrossRefGoogle Scholar
  2. Arias JA (1985) Secretary organelle and mitochondrial alterations induced by fusaric acid in root cells of Zea mays. Physiol Plant Pathol 27:149–158CrossRefGoogle Scholar
  3. Arima K, Kakinu TG, Tamura G (1968) Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation. Biochem Biophys Res Commun 31:488–494PubMedCrossRefGoogle Scholar
  4. Arshad M, Frankenberger WT (1991) Microbial production of plant hormones. In: Keister BD, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 327–334CrossRefGoogle Scholar
  5. Bacon CW, Hinton DM (2002) Endophytic and biological control potential of Bacillus mojavensis and related species. Biol Control 23:274–284CrossRefGoogle Scholar
  6. Bacon CW, Hinton DM (2006) Bacterial endophytes: the endophytic niche, its occupants, and its utility. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, The Netherlands, pp 155–194CrossRefGoogle Scholar
  7. Bacon CW, Porter JK, Norred WP, Leslie JF (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62:4039–4043PubMedGoogle Scholar
  8. Bacon CW, Yates IE, Hinton DM, Meredith F (2001) Biological control of Fusarium moniliforme in maize. Environ Health Perspect 109:325–332PubMedGoogle Scholar
  9. Bacon CW, Hinton DM, Hinton A (2006) Growth-inhibiting effects of concentrations of fusaric acid on the growth of Bacillus mojavensis and other biocontrol Bacillus species. J Appl Microbiol 100:185–194PubMedCrossRefGoogle Scholar
  10. Bacon CW, Hinton DM, Glenn AE, Macias FA, Marin D (2007) Interaction of Bacillus mojavensis and Fusarium verticillioides with a benzoxazolinone (BOA) and its transformation products, APO. J Chem Ecol 33:1885–1897PubMedCrossRefGoogle Scholar
  11. Bacon CW, Hinton DM, Mitchell TR, Snook ME, Olubajo B (2010) Surfactin production and molecular characterization of Bacillus mojavensis strains. J Biocontrol (still in review)Google Scholar
  12. Ballio A (1981) Structure-activity relationships. In: Durbin RD (ed) Toxins in plant disease. Academic, New York, pp 395–441Google Scholar
  13. Baumgart R, Kluge B, Ullrich C, Vater J, Ziessow D (1991) Identification of amino acid substitutions in the lipopeptide surfactin using 2D NMR spectroscopy. Biochem Biophys Res Commun 177:998–1005PubMedCrossRefGoogle Scholar
  14. Besson F, Tenoux I, Hourdou M, Michel G (1992) Synthesis of β-hydroxy fatty acids and β-amino acid fatty acids by strains of Bacillus subtilis producing iturinic antibiotics. Biochim Biophy Acta 1123:51–58CrossRefGoogle Scholar
  15. Bonmatin J, Laprevote O, Peypoux F (2003) Diversity among microbial cyclic lipopeptides: iturins and surfactins. Activity-structure relationships to design new bioactive agents. Comb Chem High Throughput Screen 6:541–556PubMedCrossRefGoogle Scholar
  16. Bullerman LB (1996) Occurrence of Fusarium and fumonisins on food grains and in foods. Adv Exp Med Biol 392:27–38PubMedGoogle Scholar
  17. Bungo T, Shimojo M, Masuda Y, Choi YH, Denbow DM, Furuse M (1999) Induction of food intake by a noradrenergic system using clonidine and fusaric acid in the neonatal chick. Brain Res 826:313–316PubMedCrossRefGoogle Scholar
  18. Cambier V, Hance T, De Hoffmann E (2000) Variation of DIMBOA and related compounds content in relation to the age and plant organ in maize. Phytochemistry 53:223–229PubMedCrossRefGoogle Scholar
  19. Cameotra S, Makkar R (1998) Synthesis of biosurfactants in extreme conditions. Appl Microbiol Biotechnol 50:520–529PubMedCrossRefGoogle Scholar
  20. Canny MJ (1995) Apoplastic water and solute movement: new rules for an old space. Annu Rev Plant Physiol Mol Biol 46:215–236CrossRefGoogle Scholar
  21. Chanway CP (1996) Endophytes: they’re not just fungi. Can J Bot 74:321–322CrossRefGoogle Scholar
  22. Chanway CP (1998) Bacterial endophytes: ecological and practical implications. Sydowia 50:149–170Google Scholar
  23. Cooper DG (1980) Surface active compounds from microorganisms. Adv Appl Microbiol 26:229–253CrossRefGoogle Scholar
  24. Cooper DG, MacDonald CR, Duf SFB, Kosaric N (1981) Enhances production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions. Appl Environ Microbiol 42:408–412PubMedGoogle Scholar
  25. Cooper DG, Liss SN, Longay R, Zajic JE (1989) Surface activities of Mycobacterium and Pseudomonas. J Ferment Technol 59:97–101Google Scholar
  26. Corden ME, Diamond AE (1959) The effect of growth-regulating substances on disease resistance and plant growth. Phytopathology 49:68–72Google Scholar
  27. D’Alton A, Etherton B (1984) Effects of fusaric acid on tomato root hair membrane potentials and ATP levels. Plant Physiol 74:39–42PubMedCrossRefGoogle Scholar
  28. Das K, Mukherjee AK (2006) Assessment of mosquito larvicidal potency of cyclic lipopeptides produced by Bacillus subtilis strains. Acta Trop 97:168–173PubMedCrossRefGoogle Scholar
  29. Das K, Mukherjee AK (2007) Comparison of lipopeptide biosurfactants production by Bacillus subtilis strains in submerged and solid state fermentation systems using a cheap carbon source: some industrial applications of biosurfactants. Process Biochem 42:1191–1199CrossRefGoogle Scholar
  30. Davis DA, Lynch HC, Jarley J (1999) The production of surfactin in batch culture by Bacillus subtilis ATCC 21222 is strongly influenced by the conditions of nitrogen metabolism. Enzyme Microb Technol 25:322–329CrossRefGoogle Scholar
  31. Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64PubMedGoogle Scholar
  32. Dong Z, Canny MJ, McCully ME, Roboredo MR, Cabadilla CF, Ortega E, Rodés R (1994) A nitrogen-fixing endophyte of sugarcane stems. A new role for the apoplast. Plant Physiol 105:1139–1147PubMedGoogle Scholar
  33. Drysdale RB (1984) The production and significance in phytopathology of toxins produced by species of Fusarium. In: Moss MO, Smith JE (eds) The applied mycology of Fusarium. Cambridge University Press, New York, pp 95–105Google Scholar
  34. Elbeltagy A, Suzuki H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293PubMedCrossRefGoogle Scholar
  35. Folmsbee MJ, McInerney MJ, Nagle DP (2004) Anaerobic growth of Bacillus mojavensis and Bacillus subtilis requires deoxyribonucleosides or DNA. Appl Environ Microbiol 70:5252–5257PubMedCrossRefGoogle Scholar
  36. Fomsgaard IS, Mortensen AG, Carlsen SCK (2004) Microbial transformation products of benzoxazolinone and benzoxazinone allelochemicals – a review. Chemosphere 54:1025–1038PubMedCrossRefGoogle Scholar
  37. Geetha I, Manonmani AM, Paily KP (2010) Identification and characterization of a mosquito pupicidal metabolite of a Bacillus subtilis subsp. subtilis strain. Appl Microbiol Biotechnol 86:1737–1744PubMedCrossRefGoogle Scholar
  38. Georgiou G, Lin SG, Sharma MM (1992) Surface-active compounds from microorganisms. Biotechnology 10:60–65PubMedCrossRefGoogle Scholar
  39. Glenn AE (2001) Detoxification of maize antimicrobial compounds by the endophytic fungus Fusarium verticillioides and the significance to plant-fungus interactions. Ph.D. Dissertation, University of Georgia, AthensGoogle Scholar
  40. Glenn AE, Bacon CW (1998) Detoxification of benzoxazinoids by Fusarium moniliforme and allies. Phytopathology 88:S-S32Google Scholar
  41. Glenn AE, Hinton DM, Yates IE, Bacon CW (2001) Detoxification of corn antimicrobial compounds as the basis for isolating Fusarium verticillioides and some other Fusarium species from corn. Appl Environ Microbiol 67:2973–2981PubMedCrossRefGoogle Scholar
  42. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  43. Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117–125PubMedCrossRefGoogle Scholar
  44. James EK, Olivares FL, Baldani JI, Döbereiner J (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in leaves of Sorghum bicolor L Moench. J Exp Bot 48:785–797CrossRefGoogle Scholar
  45. Javaheri M, Jenneman GE, McInerney MH, Duncan KE (1985) Anaerobic production of a biosurfactant by Bacillus licheniformis JF-2. Appl Environ Microbiol 50:698–700PubMedGoogle Scholar
  46. Joshi C, Bharucha JS, Yadav S, Nerukar A, Desai AJ (2008) Biosurfactant production using mollasses and whey under thermophilic conditions. Bioresour Technol 99:195–199PubMedCrossRefGoogle Scholar
  47. Kakinuma A, Oachida A, Shina H, Sugino M, Isano M, Tanura G, Arima K (1969) Confirmation of the structure of surfactin by mass spectrometry. Agric Biol Chem 33:1669–1672CrossRefGoogle Scholar
  48. Kikuchi T, Hasumi K (2002) Enhancement of plasminogen activation by surfactin C: augmentation of fibrinolysis in vitro and in vivo. Biochim Biophys Acta 1596:234–245PubMedCrossRefGoogle Scholar
  49. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Dekker, New York, pp 199–233Google Scholar
  50. Konz D, Doekel S, Marahiel MA (1999) Molecular and biochemical characterization of the protein template controlling biosynthesis of the lipopeptide lichenysin. J Bacteriol 181:133–140PubMedGoogle Scholar
  51. Kuklinsky-Sobral K, Araujo WL, Mendonça C, Geran LC, Pískala A, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedCrossRefGoogle Scholar
  52. Kuldau GA, Yates IE (2000) Evidence for Fusarium endophytes in cultivated and wild plants. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Dekker, New York, pp 85–117Google Scholar
  53. Kursanov AL, Brovchenko MI (1970) Sugars in the free space of leaf plates: their origin and possible involvement in transport. Can J Bot 48:1243–1250CrossRefGoogle Scholar
  54. Ladha JK, Reddy PM (1995) Introduction: assessing opportunities for nitrogen fixation in rice – a frontier project. Plant Soil 194:1–10CrossRefGoogle Scholar
  55. Landa BB, Cachinero-Díaz JM, Lemanceau P, Jiménez-Díaz RM, Alabouvette C (2002) Effect of fusaric acid and phytoanticipins on growth of rhizobacteria and Fusarium oxysporum. Can J Microbiol 48:971–985PubMedCrossRefGoogle Scholar
  56. Landy M, Warren GH, Roseman SB, Colio LG (1948) Bacillomycin: an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc Soc Exp Biol Med 67:539–541PubMedGoogle Scholar
  57. Lin S-C (1996) Biosurfactants: recent advances. J Chem Technol Biotechnol 66:109–120CrossRefGoogle Scholar
  58. Luz JM, Paterson RRM, Brayford D (1990) Fusaric acid and other metabolite production in Fusarium oxysporum f. sp. vasinfectum. Lett Appl Microbiol 11:141–144CrossRefGoogle Scholar
  59. Mace ME, Solit E (1966) Interactions of 3-indoleacetic and 3-hydroxytryamine in fusarium wilt of banana. Phytopathology 56:245–247Google Scholar
  60. MacHardy WE, Beckman CH (1981) Vascular wilt fusaria: infection and pathogenesis. In: Nelson PE, Toussoun TA, Cook RJ (eds) Fusarium: diseases, biology, and taxonomy. The Pennsylvania State University Press, University Park, pp 365–390Google Scholar
  61. Maget-Dena R, Ptak M (1995) Interfacial properties of surfactin with membrane models. Biophys J 68:1937–1943CrossRefGoogle Scholar
  62. Makkar RS, Cameotra SS (1998) Production of biosurfactants at mesophilic and thermophilic conditions by a strain of Bacillus subtilis. J Ind Microbiol Biotechnol 20:48–52CrossRefGoogle Scholar
  63. Marahiel MA, Nakano MM, Zuber P (1993) Regulation of peptide antibiotic production in Bacillus. Mol Microbiol 7:631–636PubMedCrossRefGoogle Scholar
  64. Marahiel MA, Stachelhaus T, Mootz HD (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2673PubMedCrossRefGoogle Scholar
  65. Marasas WFO, Kellerman TS, Gelderblom WCA, Coetzer JAW, Thiel PG, Van der Lugt JJ (1988) Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort J Vet Res 55:197–203PubMedGoogle Scholar
  66. Marasas WFO, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WCA, Allegood J, Martínez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill AH Jr (2004) Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134:711–716PubMedGoogle Scholar
  67. Marrè MT, Vergani P, Albergoni FG (1993) Relationship between fusaric acid uptake and its binding to cell structures by leaves of Egeria densa and its toxic effects on membrane permeability and respiration. Physiol Mol Plant Pathol 42:141–157CrossRefGoogle Scholar
  68. Matsuyama T, Kaneda K, Nakagawa Y, Isa K, Hara-Hotta J, Yano I (1992) A novel extracellular cyclic lipopeptide which promotes flagellum-dependent spreading growth of Serratia marcescens. J Bacteriol 174:1769–1776PubMedGoogle Scholar
  69. McCully ME (2001) Niches for bacterial endophytes in crop plants: a plant biologist’s view. Aust J Plant Physiol 28:983–990Google Scholar
  70. Niemeyer HM (1988) Hydroxamic acids (4-hydro-1,4-benzozazin-3-ones), defence chemical in the Gramineae. Phytochemistry 27:3349–3358CrossRefGoogle Scholar
  71. Notz R, Maurhofer M, Dubach H, Haas D, Défago G (2002) Fusaric acid-producing strains of Fusarium oxysporum alter 2,4-diacetylphloroglucinol biosynthetic gene expression in Pseudomonas fluorescens CHA0 in vitro and in the rhizosphere of wheat. Appl Environ Microbiol 68:2229–2235PubMedCrossRefGoogle Scholar
  72. Olubajo BA, Bacon CW (2008) Electrotransformation of Bacillus mojavensis with fluorescent protein markers. J Microbiol Methods 74:102–105PubMedCrossRefGoogle Scholar
  73. Patriquin DG, Dobereiner J (1978) Light microscopy observations of tetrazolium-reducing bacteria in the endorhizosphere of maize and other grasses in Brazil. Can J Microbiol 24:734–742PubMedCrossRefGoogle Scholar
  74. Peypoux E, Monmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563PubMedCrossRefGoogle Scholar
  75. Porter JK, Bacon CW, Wray EM, Hagler WM (1995) Fusaric acid in Fusarium moniliforme cultures, corn and feeds toxic to livestock and the neurochemical effects in the barin and pineal gland in rats. Nat Toxin 3:91–100Google Scholar
  76. Rahman KSM, Street G, Lord R, Kane G, Rahman TJ, Marchant R, Banat M (2006) Bioremediation of petroleum sludge using bacterial consortium with biosurfactant. In: Singh SN, Tripathi RD (eds) Environmental bioremediation technologies. Springer, Berlin, pp 391–408Google Scholar
  77. Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144PubMedCrossRefGoogle Scholar
  78. Riley RT, Norred WP, Bacon CW (1993) Fungal toxins in foods: recent concerns. Annu Rev Nutr 13:167–189PubMedCrossRefGoogle Scholar
  79. Roberts MS, Nakamura LK, Cohan FM (1994) Bacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. Int J Syst Bacteriol 44:256–264PubMedCrossRefGoogle Scholar
  80. Rodrigues L, Banat IM, Teixeira J, Oliveira R (2006) Biosurfactants: potential applications in medicine. J Antimicrob Chemother 57:609–618PubMedCrossRefGoogle Scholar
  81. Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3:229–236PubMedCrossRefGoogle Scholar
  82. Ross PF, Rice LG, Osweiler GD, Nelson PE, Richard JL, Wilson TM (1992) A review and update of animal toxicoses associated with fumonisin-contaminated feeds and production of fumonisins by Fusarium isolates. Mycopathologia 117:109–114PubMedCrossRefGoogle Scholar
  83. Sanwal BD, Waygood ER (1961) The effect of fusaric acid on the oxidative phosphorylation of plant mitochondria. Experientia 17:174–175PubMedCrossRefGoogle Scholar
  84. Schnider-Keel U, Seematter A, Maurhofer M, Blumer C, Duffy BK, Gigot-Bonnefoy C, Reimmann C, Notz R, Defago G, Hass D, Keel C (2000) Autoinduction of 2,4-diacetylphoroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescensCHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J Bacteriol 182:1215–1225PubMedCrossRefGoogle Scholar
  85. Seydlova G, Svobodova J (2008) Review of surfactin chemical properties and the potential biomedical applications. Cent Eur J Med 312:123–133CrossRefGoogle Scholar
  86. Singh HP, Batish DR, Kohli RK (2003) Allelopathic interactions and allelochemicals: new possibilities for sustainable weed management. Crit Rev Plant Sci 22:239–311CrossRefGoogle Scholar
  87. Smith TK, Sousadias MG (1993) Fusaric acid content of swine feedstuffs. J Agric Food Chem 41:2296–2298CrossRefGoogle Scholar
  88. Snook ME, Mitchell T, Hinton DM, Bacon CW (2009) Isolation and characterization of Leu7-surfactin from the endophytic bacterium Bacillus mojavensis RRC 101, a biocontrol agent for Fusarium verticillioides. Agric Food Chem 57:4287–4292CrossRefGoogle Scholar
  89. Stanghellini ME, Miller RM (1997) Biosurfactants: their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Dis 81:4012CrossRefGoogle Scholar
  90. Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30CrossRefGoogle Scholar
  91. Surette MA, Sturz AV, Lada RR, Nowak J (2003) Bacterial endophytes in processing carrots (Daucus carota L. var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant Soil 253:381–390CrossRefGoogle Scholar
  92. Thomashow LS, Weller DM (1990) Role of antibiotics and siderophores in biocontrol of take-all disease of wheat. Plant Soil 129:93–99CrossRefGoogle Scholar
  93. Von Dohren H (1995) Peptides. In: Vining LC, Stuttard C (eds) Genetics and biochemistry of antibiotic production. Butterworth-Heineman, Boston, MA, pp 121–171Google Scholar
  94. Voss KA, Porter JK, Bacon CW, Meredith FI, Norred WP (1999) Fusaric acid and modification of the subchronic toxicity to rats of fumonisins in F-moniliforme culture material. Food Chem Toxicol 37:853–861PubMedCrossRefGoogle Scholar
  95. Voss KA, Riley RT, Norred WP, Bacon CW, Meredith FI, Howard PC, Plattner RD, Collins TFX, Hansen DK, Porter JK (2001) An overview of rodent toxicities: liver and kidney effects of fumonisins and Fusarium moniliforme. Environ Health Perspect 109:259–266PubMedGoogle Scholar
  96. Whalley G (1995) Green pressures are driving force behind surfactants. Manuf Chem 11:38–40Google Scholar
  97. Whitney NJ, Mortimore CG (1959) An antifungal substance in the corn plant and its effect on growth of two stalk-rotting fungi. Nature 183:341PubMedCrossRefGoogle Scholar
  98. Yakimov MM, Fredrickson HL, Timmis KN (1996) Effect of heterogeneity of hydrophobic moieties on surface activity of lichenysin A, a lipopeptide biosurfactant from Bacillus licheniformis. Biotechnol Appl Biochem 23:13–18PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.USDA, ARS, Russell Research CenterAthensUSA

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