Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 3, pp 1179–1190 | Cite as

Cyclic lipopeptide signature as fingerprinting for the screening of halotolerant Bacillus strains towards microbial enhanced oil recovery

  • Bárbara C. S. Farias
  • Denise C. Hissa
  • Camila T. M. do Nascimento
  • Samuel A. Oliveira
  • Davila Zampieri
  • Marcos N. Eberlin
  • Deivid L. S. Migueleti
  • Luiz F. Martins
  • Maíra P. Sousa
  • Danuza N. Moyses
  • Vânia M. M. MeloEmail author
Biotechnological products and process engineering

Abstract

Cyclic lipopeptides (CLPs) are non-ribosomal biosurfactants produced by Bacillus species that exhibit outstanding interfacial activity. The synthesis of CLPs is under genetic and environmental influence, and representatives from different families are generally co-produced, generating isoforms that differ in chemical structure and biological activities. This study to evaluate the effect of low and high NaCl concentrations on the composition and surface activity of CLPs produced by Bacillus strains TIM27, TIM49, TIM68, and ICA13 towards microbial enhanced oil recovery (MEOR). The strains were evaluated in mineral medium containing NaCl 2.7, 66, or 100 g L−1 and growth, surface tension and emulsification activity were monitored. Based on the analysis of 16S rDNA, gyrB and rpoB sequences TIM27 and TIM49 were assigned to Bacillus subtilis, TIM68 to Bacillus vallismortis, and ICA13 to Bacillus amyloliquefaciens. All strains tolerated up to 100-g L−1 NaCl, but only TIM49 and TIM68 were able to reduce surface tension at this concentration. TIM49 also showed emulsification activity at concentrations up to 66-g L−1 NaCl. ESI-MS analysis showed that the strains produced a mixture of CLPs, which presented distinct CLP profiles at low and high NaCl concentrations. High NaCl concentration favored the synthesis of surfactins and/or fengycins that correlated with the surface activities of TIM49 and TIM68, whereas low concentration favored the synthesis of iturins. Taken together, these findings suggest that the determination of CLP signatures under the expected condition of oil reservoirs can be useful in the guidance for choosing well-suited strains to MEOR.

Keywords

Lipopeptides Biosurfactant Bacillus MEOR ESI-MS 

Notes

Acknowledgments

We thank André Saraiva L M Antunes for proof reading the manuscript. We acknowledge PETROBRAS for the financial support (Cooperation agreement: 0050.0079828.12.9) and authorization to publish this work and Coleção de Culturas do Gênero Bacillus e Gêneros Correlatos/FIOCRUZ for the storage of B. subtilis TIM49.

Funding information

We also thank the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for research grant provided to VMMM and doctoral scholarship to BCSF, respectively. This study was funded by PETROBRAS (grant number 0050.0079828.12.9).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2017_8675_MOESM1_ESM.pdf (151 kb)
ESM 1 (PDF 151 kb)

References

  1. Ahaotu I, Anyogu A, Njoku OH, Odu NN, Sutherland JP, Ouoba LII (2013) Molecular identification and safety of Bacillus species involved in the fermentation of African oil beans (Pentaclethra macrophylla Benth) for production of Ugba. Int J Food Microbiol 162(1):95–104.  https://doi.org/10.1016/j.ijfoodmicro.2013.01.001 CrossRefPubMedGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402.  https://doi.org/10.1093/nar/25.17.3389 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Al-Wahaibi Y, Al-Hadrami H, Al-Bahry S, Elshafie A, Al-Bemani A, Joshi S (2016) Injection of biosurfactant and chemical surfactant following hot water injection to enhance heavy oil recovery. Pet Sci 13(1):100–109.  https://doi.org/10.1007/s12182-015-0067-0 CrossRefGoogle Scholar
  4. Banat IM (1995) Biosurfactants production and possible uses in microbial enhanced oil recovery and oil pollution remediation: a review. Bioresour Technol 51(1):1–12.  https://doi.org/10.1016/0960-8524(94)00101-6 CrossRefGoogle Scholar
  5. Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R (2010) Microbial biosurfactants production , applications and future potential. Appl Microbiol Biotechnol 87(2):427–444.  https://doi.org/10.1007/s00253-010-2589-0 CrossRefPubMedGoogle Scholar
  6. Bass C, Lappin-Scott H (1997) The bad guys and the good guys in petroleum microbiology. Oilfield Rev 9:17–25Google Scholar
  7. Belyaev SS, Borzenkov IA, Nazina TN, Rozanova EP, Glumov IF, Ibatullin RR, Ivanov MV (2004) Use of microorganisms in the biotechnology for the enhancement of oil recovery. Microbiology 73(5):590–598.  https://doi.org/10.1023/B:MICI.0000044250.21076.0e CrossRefGoogle Scholar
  8. Bie X, Lu Z, Lu F (2009) Identification of fengycin homologues from Bacillus subtilis with ESI-MS/CID. J Microbiol Methods 79(3):272–278.  https://doi.org/10.1016/j.mimet.2009.09.013 CrossRefPubMedGoogle Scholar
  9. Bonmatin J-M, Laprévote 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(6):541–556.  https://doi.org/10.2174/138620703106298716 CrossRefPubMedGoogle Scholar
  10. Brown AD (1978) Compatible solutes and extreme water stress in eukaryotic micro-organisms. Adv Microb Physiol 17:181–242.  https://doi.org/10.1016/S0065-2911(08)60058-2 CrossRefPubMedGoogle Scholar
  11. Cagri-Mehmetoglu A, Kusakli S, van de Venter M (2012) Production of polysaccharide and surfactin by Bacillus subtilis ATCC 6633 using rehydrated whey powder as the fermentation medium. J Dairy Sci 95(7):3643–3649.  https://doi.org/10.3168/jds.2012-5385 CrossRefPubMedGoogle Scholar
  12. Cameotra SS, Makkar RS, Kaur J, Mehta SK (2010) Synthesis of biosurfactants and their advantages to microorganisms and mankind. Adv Exp Med Biol 672:261–280.  https://doi.org/10.1007/978-1-4419-5979-9_20 CrossRefPubMedGoogle Scholar
  13. Chakraborty J, Chakrabarti S, Das S (2014) Characterization and antimicrobial properties of lipopeptide biosurfactants produced by Bacillus subtilis SJ301 and Bacillus vallismortis JB201. Appl Biochem Microbiol 50(6):609–618.  https://doi.org/10.1134/S0003683814060039 CrossRefGoogle Scholar
  14. Chen H, Wang L, Su CX, Gong GH, Wang P, Yu ZL (2008) Isolation and characterization of lipopeptide antibiotics produced by Bacillus subtilis. Lett Appl Microbiol 47(3):180–186.  https://doi.org/10.1111/j.1472-765X.2008.02412.x CrossRefPubMedGoogle Scholar
  15. Cooper D, Macdonald C, Duff S, Kosaric N (1981) Enhanced production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions enhanced production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions. Appl Environ Microbiol 42(3):408–412PubMedPubMedCentralGoogle Scholar
  16. Dae KS, Cho JY, Park HJ, Lim CR, Lim JH, Yun HI, Park SC, Kim SK, Rhee MH (2006) A comparison of the anti-inflammatory activity of surfactin A, B, C, and D from Bacillus subtilis. J Microbiol Biotechnol 16:1656–1659Google Scholar
  17. Deleu M, Razafindralambo H, Popineau Y, Jacques P, Thonart P, Paquot M (1999) Interfacial and emulsifying properties of lipopeptides from Bacillus subtilis. Colloids Surfaces A Physicochem Eng. ASp 152(1-2):3–10.  https://doi.org/10.1016/S0927-7757(98)00627-X CrossRefGoogle Scholar
  18. Giro MEA, Martins JJL, Rocha MVP, Melo VMM, Gonçalves LRB (2009) Clarified cashew apple juice as alternative raw material for biosurfactant production by Bacillus subtilis in a batch bioreactor. Biotechnol J 4(5):738–747.  https://doi.org/10.1002/biot.200800296 CrossRefPubMedGoogle Scholar
  19. Gudiña EJ, Teixeira JA, Rodrigues LR (2010) Isolation and functional characterization of a biosurfactant produced by Lactobacillus paracasei. Colloids Surf B Biointerfaces 76(1):298–304.  https://doi.org/10.1016/j.colsurfb.2009.11.008 CrossRefPubMedGoogle Scholar
  20. Gudiña EJ, Pereira JFB, Rodrigues LR, Coutinho JAP, Teixeira JA (2012) Isolation and study of microorganisms from oil samples for application in microbial enhanced oil recovery. Int Biodeterior Biodegrad 68:56–64.  https://doi.org/10.1016/j.ibiod.2012.01.001 CrossRefGoogle Scholar
  21. Hoff E, Nyström B, Lindman B (2001) Polymer–surfactant interactions in dilute mixtures of a nonionic cellulose derivative and an anionic surfactant. Langmuir 17(1):28–34.  https://doi.org/10.1021/la001175p CrossRefGoogle Scholar
  22. Iqbal S, Khalid ZM, Malik KA (1995) Enhanced biodegradation and emulsification of crude oil and hyperproduction of biosurfactants by a gamma ray-induced mutant of Pseudomonas aeruginosa. Lett Appl Microbiol 21(3):176–179.  https://doi.org/10.1111/j.1472-765X.1995.tb01035.x CrossRefPubMedGoogle Scholar
  23. Joshi SJ, Al-Wahaibi YM, Al-Bahry SN, Elshafie AE, Al-Bemani AS, Al-Bahri A, Al-Mandhari MS (2016) Production, characterization, and application of Bacillus licheniformis W16 biosurfactant in enhancing oil recovery. Front Microbiol 7:1–14Google Scholar
  24. Kaur PK, Joshi N, Singh IP, Saini HS (2017) Identification of cyclic lipopeptides produced by Bacillus vallismortis R2 and their antifungal activity against Alternaria alternata. J Appl Microbiol 122(1):139–152.  https://doi.org/10.1111/jam.13303 CrossRefPubMedGoogle Scholar
  25. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649.  https://doi.org/10.1093/bioinformatics/bts199 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Khire JM, Khan MI (1994) Microbially enhanced oil recovery (MEOR). Part 1. Importance and mechanism of MEOR. Enzym Microb Technol 16(2):170–172.  https://doi.org/10.1016/0141-0229(94)90081-7 CrossRefGoogle Scholar
  27. Kim PI, Ryu J, Kim YH, Chi Y-T (2010) Production of biosurfactant lipopeptides iturin A, fengycin and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20(1):138–145PubMedGoogle Scholar
  28. Knoblich A, Matsumoto M, Ishiguro R, Murata K, Fujiyoshi Y, Ishigami Y, Osman M (1995) Electron cryo-microscopic studies on micellar shape and size of surfactin, an anionic lipopeptide. Colloids Surfaces B Biointerfaces 5(1-2):43–48.  https://doi.org/10.1016/0927-7765(95)01207-Y CrossRefGoogle Scholar
  29. Kowall V, Kluge S, Franke Z (1998) Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105. J Colloid Interface Sci 204(1):1–8.  https://doi.org/10.1006/jcis.1998.5558 CrossRefPubMedGoogle Scholar
  30. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  31. Lasch P, Beyer W, Nattermann H, Stammler M, Siegbrecht E, Grunow R, Naumann D (2009) Identification of Bacillus anthracis by using matrix-assisted laser desorption ionization-time of flight mass spectrometry and artificial neural networks. Appl Environ Microbiol 75(22):7229–7242.  https://doi.org/10.1128/AEM.00857-09 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Li X-Y, Mao Z-C, Wang Y-H, Wu Y-X, He Y-Q, Long C-L (2012) ESI LC-MS and MS/MS characterization of antifungal cyclic lipopeptides produced by Bacillus subtilis XF-1. J Mol Microbiol Biotechnol 22(2):83–93.  https://doi.org/10.1159/000338530 CrossRefPubMedGoogle Scholar
  33. Marchant R, Banat IM (2012) Microbial biosurfactants: challenges and opportunities for future exploitation. Trends Biotechnol 30(11):558–565.  https://doi.org/10.1016/j.tibtech.2012.07.003 CrossRefPubMedGoogle Scholar
  34. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Dymock D, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64(2):795–799PubMedPubMedCentralGoogle Scholar
  35. Marin CP, Kaschuk JJ, Frollini E, Nitschke M (2015) Potential use of the liquor from sisal pulp hydrolysis as substrate for surfactin production. Ind Crop Prod 66:239–245.  https://doi.org/10.1016/j.indcrop.2015.01.001 CrossRefGoogle Scholar
  36. Mercade ME, Manresa MA (1994) The use of agroindustrial by-products for biosurfactant production. J Am Oil Chem Soc 71(1):61–64.  https://doi.org/10.1007/BF02541473 CrossRefGoogle Scholar
  37. Mnif I, Ghribi D (2015) Lipopeptide surfactants: production, recovery and pore forming capacity. Peptides 71:100–112CrossRefGoogle Scholar
  38. Mootz HD, Marahiel MA (1997) Biosynthetic systems for nonribosomal peptide antibiotic assembly. Curr Opin Chem Biol 1(4):543–551.  https://doi.org/10.1016/S1367-5931(97)80051-8 CrossRefPubMedGoogle Scholar
  39. Morán AC, Olivera N, Commendatore M, Esteves JL, Siñeriz F (2000) Enhancement of hydrocarbon waste biodegradation by addition of a biosurfactant from Bacillus subtilis O9. Biodegradation 11(1):65–71.  https://doi.org/10.1023/A:1026513312169 CrossRefPubMedGoogle Scholar
  40. Moyne A, Cleveland TE, Tuzun S (2004) Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D. FEMS Microbiol Lett 234(1):43–49.  https://doi.org/10.1111/j.1574-6968.2004.tb09511.x CrossRefPubMedGoogle Scholar
  41. Mulligan CN (2005) Environmental applications for biosurfactants. Environ Pollut 133(2):183–198.  https://doi.org/10.1016/j.envpol.2004.06.009 CrossRefPubMedGoogle Scholar
  42. Negin C, Ali S, Xie Q (2016) Most common surfactants employed in chemical enhanced oil recovery. Petroleum 3:197–211CrossRefGoogle Scholar
  43. Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M (2012) Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79(1):176–191.  https://doi.org/10.1111/j.1574-6941.2011.01208.x CrossRefPubMedGoogle Scholar
  44. Oliveira DWF, França ÍWL, Félix AKN, Martins JJL, Giro MEA, Melo VMM, Gonçalves LRB (2013) Kinetic study of biosurfactant production by Bacillus subtilis LAMI005 grown in clarified cashew apple juice. Colloids Surfaces B Biointerfaces 101:34–43.  https://doi.org/10.1016/j.colsurfb.2012.06.011 CrossRefPubMedGoogle Scholar
  45. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16(3):115–125.  https://doi.org/10.1016/j.tim.2007.12.009 CrossRefPubMedGoogle Scholar
  46. Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4(1):2.  https://doi.org/10.1186/1746-1448-4-2 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Park K, Park Y-S, Ahamed J, Dutta S, Ryu H, Lee S-H, Balaraju K, Manir M, Moon S-S (2016) Elicitation of induced systemic resistance of chili pepper by iturin A analogs derived from Bacillus vallismortis EXTN-1. Can J Plant Sci:564–570.  https://doi.org/10.1139/cjps-2015-0199
  48. Pereira JFB, Gudiña EJ, Costa R, Vitorino R, Teixeira JA, Coutinho JAP, Rodrigues LR (2013) Optimization and characterization of biosurfactant production by Bacillus subtilis isolates towards microbial enhanced oil recovery applications. Fuel 111:259–268.  https://doi.org/10.1016/j.fuel.2013.04.040 CrossRefGoogle Scholar
  49. Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51(5):553–563.  https://doi.org/10.1007/s002530051432 CrossRefPubMedGoogle Scholar
  50. Price NPJ, Rooney AP, Swezey JL, Perry E, Cohan FM (2007) Mass spectrometric analysis of lipopeptides from Bacillus strains isolated from diverse geographical locations. FEMS Microbiol Lett 271(1):83–89.  https://doi.org/10.1111/j.1574-6968.2007.00702.x CrossRefPubMedGoogle Scholar
  51. Pueyo MT, Bloch C, Carmona-Ribeiro AM, Di Mascio P (2009) Lipopeptides produced by a soil Bacillus megaterium strain. Microb Ecol 57(2):367–378.  https://doi.org/10.1007/s00248-008-9464-x CrossRefPubMedGoogle Scholar
  52. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34(6):1037–1062.  https://doi.org/10.1111/j.1574-6976.2010.00221.x CrossRefPubMedGoogle Scholar
  53. Razafindralambo H, Popineau Y, Deleu M, Hbid C, Jacques P, Thonart P, Paquot M (1997) Surface-active properties of surfactin/iturin A mixtures produced by Bacillus subtilis. Langmuir 13(23):6026–6031.  https://doi.org/10.1021/la970533u CrossRefGoogle Scholar
  54. Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1:1–30CrossRefGoogle Scholar
  55. Roongsawang N, Thaniyavarn J, Thaniyavarn S, Kameyama T, Haruki M, Imanaka T, Morikawa M, Kanaya S (2002) Isolation and characterization of a halotolerant Bacillus subtilis BBK-1 which produces three kinds of lipopeptides: bacillomycin L, plipastatin, and surfactin. Extremophiles 6(6):499–506.  https://doi.org/10.1007/s00792-002-0287-2 CrossRefPubMedGoogle Scholar
  56. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425PubMedGoogle Scholar
  57. Samanta A, Bera A, Ojha K, Mandal A (2012) Comparative studies on enhanced oil recovery by alkali–surfactant and polymer flooding. J Pet Explor Prod Technol 2(2):67–74.  https://doi.org/10.1007/s13202-012-0021-2 CrossRefGoogle Scholar
  58. Sen R (2008) Biotechnology in petroleum recovery : the microbial EOR. Prog Energy Combust Sci 34(6):714–724.  https://doi.org/10.1016/j.pecs.2008.05.001 CrossRefGoogle Scholar
  59. Sheppard J, Mulligan C (1987) The production of surfactin by Bacillus subtilis grown on peat hydrolysate. Appl Microbiol Biotechnol 27:110–116CrossRefGoogle Scholar
  60. Sousa M, Dantas IT, Feitosa FX, Alencar AEV, Soares SA, Melo VMM, Gonçalves LRB, Sant'ana HB (2014) Performance of a biosurfactant produced by Bacillus subtilis LAMI005 on the formation of oil/biosurfactant/water emulsion: study of the phase behaviour of emulsified systems. Braz J Chem Eng 31(3):613–623.  https://doi.org/10.1590/0104-6632.20140313s00002766 CrossRefGoogle Scholar
  61. Stankovic S, Mihajlovic S, Draganic V, Dimkic I, Vukotic G, Beric T, Fira D (2012) Screening for the presence of biosynthetic genes for antimicrobial lipopeptides in natural isolates of Bacillus sp. Arch Biol Sci 64(4):1425–1432.  https://doi.org/10.2298/ABS1204425S CrossRefGoogle Scholar
  62. Stein T (2008) Whole-cell matrix-assisted laser desorption/ionization mass spectrometry for rapid identification of bacteriocin/lantibiotic-producing bacteria. Rapid Commun Mass Spectrom 22(8):1146–1152.  https://doi.org/10.1002/rcm.3481 CrossRefPubMedGoogle Scholar
  63. Suihko M-L, Stackebrandt E (2003) Identification of aerobic mesophilic bacilli isolated from board and paper products containing recycled fibres. J Appl Microbiol 94(1):25–34.  https://doi.org/10.1046/j.1365-2672.2003.01803.x CrossRefPubMedGoogle Scholar
  64. Suthar H, Hingurao K, Desai A, Nerurkar A (2008) Evaluation of bioemulsifier mediated microbial enhanced oil recovery using sand pack column. J Microbiol Methods 75(2):225–230.  https://doi.org/10.1016/j.mimet.2008.06.007 CrossRefPubMedGoogle Scholar
  65. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526PubMedGoogle Scholar
  66. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680.  https://doi.org/10.1093/nar/22.22.4673 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Vanittanakom N, Loeffler W, Koch U, Jung G (1986) Fengycin--a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiot (Tokyo) 39(7):888–901.  https://doi.org/10.7164/antibiotics.39.888 CrossRefGoogle Scholar
  68. Varadavenkatesan T, Murty VR (2013) Production of a lipopeptide biosurfactant by a novel Bacillus sp. and its applicability to enhanced oil recovery. ISRN Microbiol 2013:1–8.  https://doi.org/10.1155/2013/621519 CrossRefGoogle Scholar
  69. Vater J, Wilde C, Franke P, Mehta N, Cameotra SS (2002) Matrix-assisted laser desorption ionization–time of flight mass spectrometry of lipopeptide biosurfactants in whole cells and culture filtrates of Bacillus subtilis C-1 isolated from petroleum sludge. Appl Environ Microbiol 68(12):6210–6219.  https://doi.org/10.1128/AEM.68.12.6210-6219.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303(5665):1805–1810.  https://doi.org/10.1126/science.1094318 CrossRefPubMedGoogle Scholar
  71. Wang L-T, Lee F-L, Tai C-J, Kasai H (2007) Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA—DNA hybridization in the Bacillus subtilis group. Int J Syst Evol Microbiol 57(8):1846–1850.  https://doi.org/10.1099/ijs.0.64685-0 CrossRefPubMedGoogle Scholar
  72. Warner SAJ (1996) Genomic DNA isolation and lambda library construction. Wiley & Sons, New YorkGoogle Scholar
  73. Williams BH, Hathout Y, Fenselau C (2002) Structural characterization of lipopeptide biomarkers isolated from Bacillus globigii. J Mass Spectrom 37(3):259–264.  https://doi.org/10.1002/jms.279 CrossRefPubMedGoogle Scholar
  74. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37(Web Server):W652–W660.  https://doi.org/10.1093/nar/gkp356 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40(W1):W127–W133.  https://doi.org/10.1093/nar/gks374 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43(W1):W251–W257.  https://doi.org/10.1093/nar/gkv380 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Youssef NH, Duncan KE, McInerney MJ (2005) Importance of 3-hydroxy fatty acid composition of lipopeptides for biosurfactant activity. Appl Environ Microbiol 71(12):7690–7695.  https://doi.org/10.1128/AEM.71.12.7690-7695.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Youssef NH, Simpson DR, Duncan KE, McInerney MJ, Folmsbee M, Fincher T, Knapp RM (2007a) In situ biosurfactant production by Bacillus strains injected into a limestone petroleum reservoir. Appl Environ Microbiol 73(4):1239–1247.  https://doi.org/10.1128/AEM.02264-06 CrossRefPubMedGoogle Scholar
  79. Youssef NH, Nguyen T, Sabatini DA, McInerney MJ (2007b) Basis for formulating biosurfactant mixtures to achieve ultra low interfacial tension values against hydrocarbons. J Ind Microbiol Biotechnol 34(7):497–507.  https://doi.org/10.1007/s10295-007-0221-9 CrossRefPubMedGoogle Scholar
  80. Zhu Z, Zhang J, Wu Y, Ran W, Shen Q (2013) Comparative study on the properties of lipopeptide products and expression of biosynthetic genes from Bacillus amyloliquefaciens XZ-173 in liquid fermentation and solid-state fermentation. World J Microbiol Biotechnol 29(11):2105–2114.  https://doi.org/10.1007/s11274-013-1375-4 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Bárbara C. S. Farias
    • 1
  • Denise C. Hissa
    • 1
  • Camila T. M. do Nascimento
    • 1
  • Samuel A. Oliveira
    • 1
  • Davila Zampieri
    • 2
    • 3
  • Marcos N. Eberlin
    • 3
  • Deivid L. S. Migueleti
    • 4
  • Luiz F. Martins
    • 4
  • Maíra P. Sousa
    • 4
  • Danuza N. Moyses
    • 4
  • Vânia M. M. Melo
    • 1
    Email author
  1. 1.Laboratório de Ecologia Microbiana e Biotecnologia (LEMBiotech), Departamento de BiologiaUniversidade Federal do CearáFortalezaBrazil
  2. 2.Biocatalysis and Mass Spectrometry Research Group, Departamento de Química Orgânica e InorgânicaUniversidade Federal do CearáFortalezaBrazil
  3. 3.ThoMSon Mass Spectrometry Laboratory, Instituto de QuímicaUniversidade Estadual de CampinasSão PauloBrazil
  4. 4.Petróleo Brasileiro SA. Centro de Pesquisas e Desenvolvimento (CENPES), Expansão PDEDS/BIORio de JaneiroBrazil

Personalised recommendations