2020, Volume 6, Issue 5
Engineering >> 2020, Volume 6, Issue 5 doi: 10.1016/j.eng.2020.01.006
Rhamnolipids Induced by Glycerol Enhance Dibenzothiophene Biodegradation in Burkholderia sp. C3
Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, Honolulu, HI 96822, USA
Next Previous
Abstract
In highly urbanized areas, pollution from anthropogenic activities has compromised the integrity of the land, decreasing soil availability for agricultural practices. Dibenzothiophene (DBT) is a heterocyclic aromatic hydrocarbon frequently found in urbanized areas, and is often used as a model chemical to study the microbial transformation of pollutants. The potential for human exposure and its health risk makes DBT a chemical of concern; thus, it needs to be environmentally managed. We utilized glycerol to stimulate Burkholderia sp. C3 in order to degrade DBT in respect to ① DBT biodegradation kinetics, ② bacterial growth, ③ rhamnolipid (RL) biosynthesis, and ④ RL secretion. Under an optimum glycerol-to-DBT molar ratio, the DBT biodegradation rate constants increased up to 18-fold and enhanced DBT biodegradation by 25%–30% at day 1 relative to cultivation with DBT alone. This enhancement was correlated with an increase in bacterial growth and RL biosynthesis. Proteomics studies revealed the enzymes involved in the upper and main steps of RL biosynthesis. The RL congeners Rha-C10-C10, Rha-Rha-C10-C10, Rha-Rha-C10-C12, and Rha-Rha-C12-C12 were identified in the medium supplemented with glycerol and DBT, whereas only Rha-C12-C12 was identified in cultures without glycerol or with RL inhibitors. The studies indicated that glycerol enhances DBT biodegradation via increased RL synthesis and bacterial growth. The results warrant further studies of environmental biostimulation with glycerol to advance bioremediation technologies and increase soil availability for agricultural purposes.
Keywords
Biodegradation ; Bioremediation ; Biosurfactant ; Biotransformation ; Glycerol ; Microbial metabolism ; Rhamnolipid
Figures
Fig. 1
Fig. 2
Fig. 3
Fig. 4
References
[ 1 ] Kampman B, Brouwer F, Schepersa B. Agricultural land availability and demand in 2020: a global analysis of drivers and demand for feedstock, and agricultural land availability. Delft: CE Delft; 2008. link1
[ 2 ] Gereslassie T, Workineh A, Liu X, Yan X, Wang J. Occurrence and ecological and human health risk assessment of polycyclic aromatic hydrocarbons in soils from Wuhan, central China. Int J Environ Res Public Health 2018;15(12): E2751. link1
[ 3 ] Lim MW, Lau EV, Poh PE. A comprehensive guide of remediation technologies for oil contaminated soil—present works and future directions. Mar Pollut Bull 2016;109(1):14–45. link1
[ 4 ] Andreolli M, Lampis S, Poli M, Gullner G, Biró B, Vallini G. Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere 2013;92(6):688–94. link1
[ 5 ] Li M, Wang TG, Simoneit BR, Shi S, Zhang L, Yang F. Qualitative and quantitative analysis of dibenzothiophene, its methylated homologues, and benzonaphthothiophenes in crude oils, coal, and sediment extracts. J Chromatogr A 2012;1233:126–36. link1
[ 6 ] Incardona JP, Collier TK, Scholz NL. Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 2004;196(2):191–205. link1
[ 7 ] Seo JS, Keum YS, Li QX. Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 2009;6(1):278–309. link1
[ 8 ] Brinkmann M, Maletz S, Krauss M, Bluhm K, Schiwy S, Kuckelkorn J, et al. Heterocyclic aromatic hydrocarbons show estrogenic activity upon metabolization in a recombinant transactivation assay. Environ Sci Technol 2014;48(10):5892–901. link1
[ 9 ] Li F, Zhu L, Wang L, Zhan Y. Gene expression of an arthrobacter in surfactantenhanced biodegradation of a hydrophobic organic compound. Environ Sci Technol 2015;49(6):3698–704. link1
[10] Demanèche S, Meyer C, Micoud J, Louwagie M, Willison JC, Jouanneau Y. Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol 2004;70(11):6714–25. link1
[11] Singleton DR, Hu J, Aitken MD. Heterologous expression of polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase genes from a novel pyrenedegrading betaproteobacterium. Appl Environ Microbiol 2012;78(10):3552–9. link1
[12] Eibes G, Cajthaml T, Moreira MT, Feijoo G, Lema JM. Enzymatic degradation of anthracene, dibenzothiophene and pyrene by manganese peroxidase in media containing acetone. Chemosphere 2006;64(3):408–14. link1
[13] Szulc A, Ambrozewicz D, Sydow M, Ławniczak Ł, Piotrowska-Cyplik A, Marecik _ R, et al. The influence of bioaugmentation and biosurfactant addition on bioremediation efficiency of diesel-oil contaminated soil: feasibility during field studies. J Environ Manage 2014;132:121–8. link1
[14] Noordman WH, Janssen DB. Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 2002;68 (9):4502–8. link1
[15] Makkar RS, Rockne KJ. Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 2003;22(10):2280–92. link1
[16] Elliot R, Singhal N, Swift S. Surfactants and bacterial bioremediation of polycyclic aromatic hydrocarbon contaminated soil—unlocking the targets. Crit Rev Environ Sci Technol 2010;41(1):78–124. link1
[17] Perfumo A, Banat IM, Canganella F, Marchant R. Rhamnolipid production by a novel thermophilic hydrocarbon-degrading Pseudomonas aeruginosa AP02-1. Appl Microbiol Biotechnol 2006;72(1):132. link1
[18] Peng F, Liu Z, Wang L, Shao Z. An oil-degrading bacterium: Rhodococcus erythropolis strain 3C–9 and its biosurfactants. J Appl Microbiol 2007;102 (6):1603–11. link1
[19] Xia W, Du Z, Cui Q, Dong H, Wang F, He P, et al. Biosurfactant produced by novel Pseudomonas sp. WJ6 with biodegradation of n-alkanes and polycyclic aromatic hydrocarbons. J Hazard Mater 2014;276:489–98. link1
[20] Bodour AA, Drees KP, Maier RM. Distribution of biosurfactant-producing bacteria in undisturbed and contaminated arid southwestern soils. Appl Environ Microbiol 2003;69(6):3280–7. link1
[21] Seo JS, Keum YS, Harada RM, Li QX. Isolation and characterization of bacteria capable of degrading polycyclic aromatic hydrocarbons (PAHs) and organophosphorus pesticides from PAH-contaminated soil in Hilo, Hawaii. J Agric Food Chem 2007;55(14):5383–9. link1
[22] Tittabutr P, Cho IK, Li QX. Phn and Nag-like dioxygenases metabolize polycyclic aromatic hydrocarbons in Burkholderia sp. C3. Biodegradation 2011;22(6):1119–33. link1
[23] Seo JS, Keum YS, Hu Y, Lee SE, Li QX. Degradation of phenanthrene by Burkholderia sp. C3: initial 1,2- and 3,4-dioxygenation and meta- and orthocleavage of naphthalene-1,2-diol. Biodegradation 2007;18(1):123–31. link1
[24] Abdel-Mawgoud AM, Lépine F, Déziel E. A stereospecific pathway diverts ß- oxidation intermediates to the biosynthesis of rhamnolipid biosurfactants. Chem Biol 2014;21(1):156–64. link1
[25] Gutierrez M, Choi MH, Tian B, Xu J, Rho JK, Kim MO, et al. Simultaneous inhibition of rhamnolipid and polyhydroxyalkanoic acid synthesis and biofilm formation in Pseudomonas aeruginosa by 2-bromoalkanoic acids: effect of inhibitor alkyl-chain-length. PLoS ONE 2013;8(9):e73986. link1
[26] Bastiaens L, Springael D, Wattiau P, Harms H, deWachter R, Verachtert H, et al. Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 2000;66 (5):1834–43. link1
[27] Akhtar N, Ghauri MA, Anwar MA, Akhtar K. Analysis of the dibenzothiophene metabolic pathway in a newly isolated Rhodococcus spp. FEMS Microbiol Lett 2009;301(1):95–102. link1
[28] Dephoure N, Gygi SP. A solid phase extraction-based platform for rapid phosphoproteomic analysis. Methods 2011;54(4):379–86. link1
[29] Tabb DL, Fernando CG, Chambers MC. MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J Proteome Res 2007;6(2):654–61. link1
[30] Ma ZQ, Dasari S, Chambers MC, Litton MD, Sobecki SM, Zimmerman LJ, et al. IDPicker 2.0: improved protein assembly with high discrimination peptide identification filtering. J Proteome Res 2009;8(8):3872–81. link1
[31] Holman JD, Ma ZQ, Tabb DL. Identifying proteomic LC-MS/MS data sets with bumbershoot and IDPicker. Curr Protoc Bioinf 2012;37(1):13–7. link1
[32] Griffin NM, Yu J, Long F, Oh P, Shore S, Li Y, et al. Label-free, normalized quantification of complex mass spectrometry data for proteomic analysis. Nat Biotechnol 2010;28(1):83–9. link1
[33] Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014;15(12):550. link1
[34] Irie Y, Parsek MR. LC/MS/MS-based quantitative assay for the secondary messenger molecule, c-di-GMP. Pseudomonas Methods Protoc 2014; 1149:271–9. link1
[35] Laabei M, Jamieson WD, Lewis SE, Diggle SP, Jenkins AT. A new assay for rhamnolipid detection-important virulence factors of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 2014;98(16):7199–209. link1
[36] Price NP, Ray KJ, Vermillion K, Kuo TM. MALDI-TOF mass spectrometry of naturally occurring mixtures of monorhamnolipids and dirhamnolipids. Carbohydr Res 2009;344(2):204–9. link1
[37] Price NP. Oligosaccharide structures studied by hydrogen-deuterium exchange and MALDI-TOF mass spectrometry. Anal Chem 2006;78(15):5302–8. link1
[38] Abdel-Mawgoud AM, Lépine F, Déziel E. Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 2010;86 (5):1323–36. link1
[39] Hennessee CT, Li QX. Effects of polycyclic aromatic hydrocarbon mixtures on degradation, gene expression, and metabolite production in four Mycobacterium species. Appl Environ Microbiol 2016;82(11):3357–69. link1
[40] Deutscher J. The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 2008;11(2):87–93. link1
[41] Wolfe A, Shimer GH Jr, Meehan T. Polycyclic aromatic hydrocarbons physically intercalate into duplex regions of denatured DNA. Biochemistry 1987;26 (20):6392–6. link1
[42] Dabestani R, Ivanov IN. A compilation of physical, spectroscopic and photophysical properties of polycyclic aromatic hydrocarbons. Photochem Photobiol 1999;70(1):10–34. link1
[43] Dobler L, Vilela LF, Almeida RV, Neves BC. Rhamnolipids in perspective: gene regulatory pathways, metabolic engineering, production and technological forecasting. N Biotechnol 2016;33(1):123–35. link1
[44] Costa SG, Déziel E, Lépine F. Characterization of rhamnolipid production by Burkholderia glumae. Lett Appl Microbiol 2011;53(6):620–7. link1
[45] Choi MH, Xu J, Gutierrez M, Yoo T, Cho YH, Yoon SC. Metabolic relationship between polyhydroxyalkanoic acid and rhamnolipid synthesis in Pseudomonas aeruginosa: comparative 13C NMR analysis of the products in wild-type and mutants. J Biotechnol 2011;151(1):30–42. link1
[46] Rehm BH, Mitsky TA, Steinbüchel A. Role of fatty acid de novo biosynthesis in polyhydroxyalkanoic acid (PHA) and rhamnolipid synthesis by pseudomonads: establishment of the transacylase (PhaG)-mediated pathway for PHA biosynthesis in Escherichia coli. Appl Environ Microbiol 2001;67 (7):3102–9. link1
[47] Zhu K, Rock CO. RhlA converts ß-hydroxyacyl-acyl carrier protein intermediates in fatty acid synthesis to the ß-hydroxydecanoyl- ß-hydroxydecanoate component of rhamnolipids in Pseudomonas aeruginosa. J Bacteriol 2008;190(9):3147–54. link1
[48] Tavares LF, Silva PM, Junqueira M, Mariano DC, Nogueira FC, Domont GB, et al. Characterization of rhamnolipids produced by wild-type and engineered Burkholderia kururiensis. Appl Microbiol Biotechnol 2013;97 (5):1909–21. link1
[49] Ochsner UA, Reiser J, Fiechter A, Witholt B. Production of Pseudomonas aeruginosa rhamnolipid biosurfactants in heterologous hosts. Appl Environ Microbiol 1995;61(9):3503–6. link1
[50] Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P, Lam JS, et al. Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol Microbiol 2001;40(3):708–18. link1
[51] Déziel E, Lépine F, Milot S, Villemur R. Mass spectrometry monitoring of rhamnolipids from a growing culture of Pseudomonas aeruginosa strain 57RP. Biochim Biophys Acta Mol Cell Biol Lipids 2000;1485(2–3):145–52. link1
京公网安备 11010502051620号
