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Hexadecane and Hexadecane-Degrading Bacteria: Mechanisms of Interaction

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Abstract

The review presents the results of investigation of the interaction between the hydrophobic substrate hexadecane and microbial cells. Three aspects of this process are discussed in more detail: (1) interaction of bacterial cells with the hydrophobic substrate, including characteristics of the cell surface and the conformational changes occurring at contact between the cell and the insoluble substrate; (2) molecular basics of the degradation of hydrophobic compounds at each stage of the cell–substrate interaction, such as synthesis of dispersing components, dispersion of the water-insoluble substrate, sorption of the hydrophobic compound by the cell and its storage, as well as transcription regulation of the genes involved either directly in biodegradation or in the processes associated with growth on hydrophobic substrates; and (3) bacterial synthesis of surfactants in the course of the degradation of hydrophobic compounds, diversity of their structure and conditions for their enhance release, as well as their biotechnological application.

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REFERENCES

  1. Agarwal, A. and Liu, Y., Remediation technologies for oil-contaminated sediments, Mar. Pollut. Bull., 2015, vol. 101, pp. 483–490.

    Article  CAS  PubMed  Google Scholar 

  2. Arelli, A., Nuzzo, A., Sabia, C., Banat, I.M., Zanaro-lia, G., and Fava, F., Optimization of washing conditions with biogenic mobilizing agents for marine fuel-contaminated beach sands, New Biothech., 2018, vol. 43, pp. 13–22.

    Article  CAS  Google Scholar 

  3. Atlas, R.M. and Hazen, T.C., Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history, Environ. Sci. Technol., 2011, vol. 45, pp. 6709‒6715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bak, F., Bonnichsen, L., Jørgensen, N.O., Nicolai-sen, M.H., and Nybroe, O., The biosurfactant viscosin transiently stimulates n-hexadecane mineralization by a bacterial consortium, Appl. Microbiol. Biotechnol., 2015, vol. 99, pp. 1475‒1483.

    Article  CAS  PubMed  Google Scholar 

  5. Bendinger, B., Rijnaarts, H.H., Altendorf, K., and Zehnder, A.J., Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence and chain length of mycolic acids, Appl. Environ. Microbiol., 1993, vol. 59, pp. 3973‒3977.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bouchez-Naïtali, M., Blanchet, D., Bardin, V., and Vandecasteele, J.P., Evidence for interfacial uptake in hexadecane degradation by Rhodococcus equi: the importance of cell flocculation, Microbiology (UK), 2001, vol. 147, pp. 2537‒2543.

    Article  Google Scholar 

  7. Cameotra, S.S. and Singh, P., Synthesis of rhamnolipid biosurfactant and mode of hexadecane uptake by Pseudomonas species, Microb. Cell Fact, 2009, vol. 8, p. 16. https://doi.org/10.1186/1475-2859-8-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen, Y., Busscher, H.J., van der Mei, H.C., and Norde, W., Statistical analysis of long- and short-range forces involved in bacterial adhesion to substratum surfaces as measured using atomic force microscopy, Appl. Environ. Microbiol., 2011, vol. 77, pp. 5065‒5070.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chen, Y., Harapanahalli, AK., Busscher, H.J., Norde, W., and van der Mei, H.C., Nanoscale cell wall deformation impacts long-range bacterial adhesion forces on surfaces, Appl. Environ. Microbiol., 2014, vol. 80, pp. 637‒643.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cheng, L., Ding, C., Li, Q., He, Q., Dai, L.R., and Zhang, H., DNA-SIP reveals that Syntrophaceae play an important role in methanogenic hexadecane degradation, PLoS One, 2013, vol. 8. e 66784. https://doi.org/10.1371/journal.pone.0066784

  11. Christova, N., Lang, S., Wray, V., Kaloyanov, K., Konstantinov, S., and Stoineva, I., Production, structural elucidation, and in vitro antitumor activity of trehalose lipid biosurfactant from Nocardia farcinica strain, J. Microbiol. Biotechnol., 2015, vol. 25, pp. 439–447.

    Article  CAS  PubMed  Google Scholar 

  12. Deziel, E., Comeau, Y., and Villemur, R., Two-liquid-phase bioreactors for enhanced degradation of hydrophobic/toxic compounds, Biodegradation, 1999, vol. 10, pp. 219–233.

    Article  CAS  PubMed  Google Scholar 

  13. Dong, Y., Yan, J., Du, H., Chen, M., Ma, T., and Feng, L., Engineering of LadA for enhanced hexadecane oxidation using random- and site-directed mutagenesis, Appl. Microbiol. Biotechnol., 2012, vol. 94, pp. 1019‒1029.

    Article  CAS  PubMed  Google Scholar 

  14. Franzetti, A., Gandolfi, I., Bestetti, G., Smyth, T.J.P., and Banat, I.M., Production and applications of trehalose lipid biosurfactants, Eur. J. Lipid Sci. Technol., 2010, vol. 112, pp. 617–627.

    Article  CAS  Google Scholar 

  15. Gudiña, E.J., Pereira, J.F., Costa, R., Evtuguin, D.V., Coutinho, J.A., Teixeira, J.A., and Rodrigues, L.R., Novel bioemulsifier produced by a Paenibacillus strain isolated from crude oil, Microb. Cell Fact, 2015, vol. 14, p. 14. https://doi.org/10.1186/s12934-015-0197-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Harapanahalli, A.K., Younes, J.A., Allan, E., van der Mei, H.C., and Busscher, H.J., Chemical signals and mechanosensing in bacterial responses to their environment, PLoS Pathog., 2015a, vol. 11. e1005057. https://doi.org/10.1371/journal.ppat.1005057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Harapanahalli, A.K., Chen, Y., Li, J., Busscher, H.J., and van der Mei, H.C., Influence of adhesion force on icaA and cidA gene expression and production of matrix components in Staphylococcus aureus biofilms, Appl. Environ. Microbiol., 2015b, vol. 81, pp. 3369‒3378.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hori, K., Watanabe, H., Ishii, S., Tanji, Y., and Unno, H., Monolayer adsorption of a “bald” mutant of the highly adhesive and hydrophobic bacterium Acinetobacter sp. strain Tol 5 to a hydrocarbon surface, Appl. Environ. Microbiol., 2008, vol. 74, pp. 2511‒2517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hua, X., Wu, Z., Zhang, H., Lu, D., Wang, M., Liu, Y., and Liu, Z., Degradation of hexadecane by Enterobacter cloacae strain TU that secretes an exopolysaccharide as a bioemulsifier, Chemosphere, 2010, vol. 80, pp. 951‒956.

    Article  CAS  PubMed  Google Scholar 

  20. Inaba, T., Tokumoto, Y., Miyazaki, Y., Inoue, N., Maseda, H., Nakajima-Kambe, T., Uchiyama, H., and Nomura, N., Analysis of genes for succinoyl trehalose lipid production and increasing production in Rhodococcus sp. strain SD-74, Appl. Environ. Microbiol., 2013, vol. 79, pp. 7082–7090.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Jung, J., Noh, J., and Park, W., Physiological and metabolic responses for hexadecane degradation in Acinetobacter oleivorans DR1, J. Microbiol., 2011, vol. 49, pp. 208–215.

    Article  CAS  PubMed  Google Scholar 

  22. Kang, Y.S. and Park, W., Contribution of quorum-sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1, J. Appl. Microbiol., 2010, vol. 109, pp. 1650‒1659.

    CAS  PubMed  Google Scholar 

  23. Kim, J.H., Kim, S.H., Yoon, J.H., and Lee, P.C., Carotenoid production from n-alkanes with a broad range of chain lengths by the novel species Gordonia ajoucoccus A2(T), Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 3759‒3768.

    Article  CAS  PubMed  Google Scholar 

  24. Kirscher, Z.I., Rosenberg, E., and Gutnic, D., Incorpora-tion of 32P and growth of Pseudomonad UP-2 on n-tetracosane, Appl. Environ. Microbiol., 1980, vol. 40, pp. 1086‒1093.

    Google Scholar 

  25. Klein, B., Bouriat, P., Goulas, P., and Grimaud, R., Behavior of Marinobacter hydrocarbonoclasticus SP17 cells during initiation of biofilm formation at the alkane-water interface, Biotechnol. Bioeng., 2010, vol. 105, pp. 461–468.

    Article  CAS  PubMed  Google Scholar 

  26. Kvenvolden, K.A. and Cooper, C.K., Natural seepage of crude oil into the marine environment, Geo-Mar. Lett., 2003, vol. 23, pp. 140–146.

    Article  CAS  Google Scholar 

  27. Laczi, K., Kis, Á., Horváth, B., Maróti, G., Hegedüs, B., Perei, K., and Rákhely, G., Metabolic responses of Rhodococcus erythropolis PR4 grown on diesel oil and various hydrocarbons, Appl. Microbiol. Biotechnol., 2015, vol. 99, pp. 9745‒9759.

    Article  CAS  PubMed  Google Scholar 

  28. Liang, X., Liao, C., Thompson, M.L., Soupir, M.L., Jarboe, L.R., and Dixon, P.M., E. coli surface properties differ between stream water and sediment environments, Front. Microbiol., 2016, vol. 7, p. 1732.

    PubMed  PubMed Central  Google Scholar 

  29. Liang, T.W. and Wang, S.L., Recent advances in exopolysaccharides from Paenibacillus spp.: production, isolation, structure, and bioactivities, Mar. Drugs, 2015, vol. 13, pp. 1847‒1863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lo Piccolo, L., De Pasquale, C., Fodale, R., Puglia, A.M., and Quatrini, P., Involvement of an alkane hydroxylase sys-tem of Gordonia sp. strain SoCg in degradation of solid n-alkanes, Appl. Environ. Microbiol., 2011, vol. 77, pp. 1204‒1213.

    Article  CAS  PubMed  Google Scholar 

  31. Mao, X, Jiang, R, Xiao, W, and Yu, J., Use of surfactants for the remediation of contaminated soils: a review, J. Hazard. Mater., 2015, vol. 285, pp. 419–435.

    Article  CAS  PubMed  Google Scholar 

  32. Mishra, S. and Singh, S.N., Microbial degradation of n‑hexadecane in mineral salt medium as mediated by degradative enzymes, Bioresour. Technol., 2012, vol. 111, pp. 148‒154.

    Article  CAS  PubMed  Google Scholar 

  33. Mounier, J., Camus, A., Mitteau, I., Vaysse, P.J., Goulas, P., Grimaud, R., and Sivadon, P., The marine bacterium Marinobacter hydrocarbonoclasticus SP17 degrades a wide range of lipids and hydrocarbons through the formation of oleolytic biofilms with distinct gene expression profiles, FEMS Microbiol. Ecol., 2014, vol. 90, pp. 816‒831.

    Article  CAS  PubMed  Google Scholar 

  34. Naether, D.J., Slawtschew, S., Stasik, S., Engel, M., Olzog, M., Wick, L.Y., Timmis, K.N., and Heipieper, H.J., Adaptation of the hydrocarbonoclastic bacterium Alcanivorax borkumensis SK2 to alkanes and toxic organic compounds: a physiological and transcriptomic approach, Appl. Environ. Microbiol., 2013, vol. 79, pp. 4282‒4293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Navon-Venezia, S., Zosim, Z., Gottlieb, A., Legmann, R., Carmeli, S., Ron, E., and Rosenberg, E., Alasan, a new bioemulsifier from Acinetobacter radioresistens, Appl. Environ. Microbiol., 1995, vol. 61, pp. 3240–3244.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Nie, H., Nie, M., Xiao, T., Wang, Y., and Tian, X., Hexadecane degradation of Pseudomonas aeruginosa NY3 promoted by glutaric acid, Sci. Total Environ., 2017, vol. 575, pp. 1423‒1428.

    Article  CAS  PubMed  Google Scholar 

  37. Paniagua-Michel, J.de J., Olmos-Soto, J., and Morales-Guerrero, E.R., Algal and microbial exopolysaccharides: new insights as biosurfactants and bioemulsifiers, Adv. Food Nutr. Res., 2014, vol. 73, pp. 221‒257.

    Article  CAS  Google Scholar 

  38. Paria, S., Surfactant-enhanced remediation of organic contaminated soil and water, Adv. Colloid Interface Sci., 2008, vol. 138, pp. 24–58.

    Article  CAS  PubMed  Google Scholar 

  39. Pathak, M., Sarma, H.K., Bhattacharyya, K.G., Subudhi, S., Bisht, V., La, B., and Devi, A., Characterization of a novel polymeric bioflocculant produced from bacterial utilization of n-hexadecane and its application in removal of heavy metals, Front. Microbiol., 2017, vol. 8. Article 170. https://doi.org/10.3389/fmicb.2017.00170

    Article  PubMed  PubMed Central  Google Scholar 

  40. Pepi, M., Cesàro, A., Liut, G., and Baldi, F., An antarctic psychrotrophic bacterium Halomonas sp. ANT-3b, growing on n-hexadecane, produces a new emulsyfying glycolipid, FEMS Microbiol. Ecol., 2005, vol. 53, pp. 157‒166.

    Article  PubMed  Google Scholar 

  41. Perry, M.B., MacLean, L.L., Patrauchan, M.A., and Vinogradov, E., The structure of the exocellular polysaccharide produced by Rhodococcus sp. RHA1, Carbohydr. Res., 2007, vol. 342, pp. 2223–2229.

    Article  CAS  PubMed  Google Scholar 

  42. Petrikov, K.V., Delegan, Ya.A., Surin, A., Ponamoreva, O.N., Puntus, I.F., Filonov, A.E., and Boronin, A.M., Glycolipids of Pseudomonas and Rhodococcus oil-degrading bacteria used in bioremediation preparations: formation and structure, Process Biochem., 2013, vol. 48, pp. 931–935.

    Article  CAS  Google Scholar 

  43. Pirog, T.P., Shevchuk, T.A., and Klimenko, Iu.A., Intensification of surfactant synthesis in Rhodococcus erythropolis EK-1 cultivated on hexadecane, Appl. Biochem. Microbiol., 2010, vol. 46, pp. 599‒606.

    Article  CAS  Google Scholar 

  44. Pirog, T.P. and Ignatenko, S.V. Scaling of the process of biosynthesis of surfactants by Rhodococcus erythropolis EK-1 on hexadecane, Appl. Biochem. Microbiol., 2011, vol. 47, pp. 393‒399.

    Article  CAS  Google Scholar 

  45. Procópio, L., de Cassia Pereira e Silva, M., van Elsas, J.D., and Seldin, L., Transcriptional profiling of genes involved in n-hexadecane compounds assimilation in the hydrocarbon degrading Dietzia cinnamea P4 strain, Braz. J. Microbiol., 2013, vol. 44, pp. 633‒641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Rabus, R., Boll, M., Heider, J., Meckenstock, R.U., Buckel, W., Einsle, O., Ermler, U., Golding, B.T., Gunsalus, R.P., Kroneck, P.M., Krüger, M., Lueders, T., Martins, B.M., Musat, F., Richnow, H.H., et al., Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment, J. Mol. Microbiol. Biotechnol., 2016, vol. 26, pp. 5‒28.

    Article  CAS  PubMed  Google Scholar 

  47. Regina, V.R., Lokanathan, A.R., Modrzyński, J.J., Sutherland, D.S., and Meyer, R.L., Surface physicochemistry and ionic strength affects eDNA’s role in bacterial adhesion to abiotic surfaces, PLoS One, 2014, vol. 9. e105033. https://doi.org/10.1371/journal.pone.0105033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Rosenberg, E. and Ron, E.Z., High- and low-molecular-mass microbial surfactants, Appl. Microbiol. Biotechnol., 1999, vol. 52, pp. 154–162.

    Article  CAS  PubMed  Google Scholar 

  49. Rubtsova, E.V., Kuiukina, M.S., and Ivshina, I.B., Effect of cultivation conditions on the adhesive activity of rhodococci towards n-hexadecane, Appl. Biochem. Microbiol., 2012, vol. 48, pp. 452‒459.

    Article  CAS  Google Scholar 

  50. Sameshima, Y., Honda, K., Kato, J., Omasa, T., and Ohtake, H., Expression of Rhodococcus opacus alkB genes in anhydrous organic solvents, J. Biosci. Bioeng., 2008, vol. 106, pp. 199–203.

    Article  CAS  PubMed  Google Scholar 

  51. Stenström, T.A., Bacterial hydrophobicity, an overall parameter for the measurement of adhesion potential to soil particles, Appl. Environ. Microbiol., 1989, vol. 55, pp. 142‒147.

    PubMed  PubMed Central  Google Scholar 

  52. Sun, J.Q., Xu, L., Tang, Y.Q., Chen, F.M., and Wu, X.L., Simultaneous degradation of phenol and n-hexadecane by Acinetobacter strains, Bioresour. Technol., 2012, vol. 123, pp. 664‒668.

    Article  CAS  PubMed  Google Scholar 

  53. Tokumoto, Y., Nomura, N., Uchiyama, H., Imura, T., Morita, T., Fukuoka, T., and Kitamoto, D., Structural characterization and surface-active properties of a succinoyl trehalose lipid produced by Rhodococcus sp. SD-74, J. Oleo Sci., 2009, vol. 58, pp. 97–102.

    Article  CAS  PubMed  Google Scholar 

  54. Toth, C.R.A. and Gieg, L.M., Time course-dependent methanogenic crude oil biodegradation: dynamics of fumarate addition metabolites, biodegradative genes, and microbial community composition, Front. Microbiol., 2018, vol. 8, p. 2610. https://doi.org/10.3389/fmicb.2017.02610

    Article  PubMed  PubMed Central  Google Scholar 

  55. Tuleva, B., Christova, N., Cohen, R., Stoev, G., and Stoineva, I., Production and structural elucidation of trehalose tetraesters (biosurfactants) from a novel alkanothrophic Rhodococcus wratislaviensis strain, J. Appl. Microbiol., 2008, vol. 104, pp. 1703–1710.

    Article  CAS  PubMed  Google Scholar 

  56. Urai, M., Yoshizaki, H., Anzai, H., Ogihara, J., Iwabuchi, N., Harayama, S., Sunairi, M., and Nakajima, M., Structural analysis of an acidic, fatty acid ester-bonded extracellular polysaccharide produced by a pristane-assimilating marine bacterium, Rhodococcus erythropolis PR4, Carbohydr. Res., 2007a, vol. 342, pp. 933–942.

    Article  CAS  PubMed  Google Scholar 

  57. Urai, M., Yoshizaki, H., Anzai, H., Ogihara, J., Iwabuchi, N., Harayama, S., Sunairi, M., and Nakajima, M., Structural analysis of mucoidan, an acidic extracellular polysaccharide produced by a pristaneassimilating marine bacterium, Rhodococcus erythropolis PR4, Carbohydr. Res., 2007b, vol. 342, pp. 927–932.

    Article  CAS  PubMed  Google Scholar 

  58. Vaysse, P.J., Prat, L., Mangenot, S., Cruveiller, S., Goulas, P., and Grimaud, R., Proteomic analysis of Marinobacter hydrocarbonoclasticus SP17 biofilm formation at the alkane-water interface reveals novel proteins and cellular processes involved in hexadecane assimilation, Res. Microbiol., 2009, vol. 160, pp. 829‒837.

    Article  CAS  PubMed  Google Scholar 

  59. White, D.A., Hird, L.C., and Ali, S.T., Production and characterization of a trehalolipid biosurfactant produced by the novel marine bacterium Rhodococcus sp., strain PML026, J. Appl. Microbiol., 2013, vol. 115, pp. 744–755.

    Article  CAS  PubMed  Google Scholar 

  60. Whyte, L.G., Smits, T.H.M., Labbé, D., Witholt, B., Greer, C.W., and van Beilen, J.B., Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531, Appl. Environm. Microbiol., 2002, vol. 68, pp. 5933–5942.

    Article  CAS  Google Scholar 

  61. Wu, B., Lan, T., Lu, D., and Liu, Z., Ecological and enzymatic responses to petroleum contamination, Environ Sci. Process Impacts, 2014, vol. 16, pp. 1501‒1509.

    Article  CAS  PubMed  Google Scholar 

  62. Xu, H.L., Chen, J.N., Wang, S.D., and Liu, Y., Oil spill forecast model based on uncertainty analysis: a case study of Dalian oil spill, Ocean Eng., 2012, vol. 54, pp. 206‒212.

    Article  Google Scholar 

  63. Zampolli, J., Collina, E., Lasagni, M., and Di Gennaro, P., Biodegradation of variable-chain-length n-alkanes in Rhodococcus opacus R7 and the involvement of an alkane hydroxylase system in the metabolism, AMB Express, 2014, vol. 4, p. 73. https://doi.org/10.1186/s13568-014-0073-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Zhao, Y.H., Chen, L.Y., Tian, Z.J., Sun, Y., Liu, J.B., and Huang, L., Characterization and application of a novel bioemulsifier in crude oil degradation by Acinetobacter beijerinckii ZRS, J. Basic Microbiol., 2016, vol. 56, pp. 184‒195.

    Article  CAS  PubMed  Google Scholar 

  65. Zeng, G., Liu, Z., Zhong, H., Li, J., Yuan, X., Fu, H., Ding, Y., Wang, J., and Zhou, M., Effect of monorhamnolipid on the degradation of n-hexadecane by Candida tropicalis and the association with cell surface properties, Appl. Microbiol. Biotechnol., 2011, vol. 90, pp. 1155‒1161.

    Article  CAS  PubMed  Google Scholar 

  66. Zheng, C., Li, Z., Su, J., Zhang, R., Liu, C., and Zhao, M., Characterization and emulsifying property of a novel bioemulsifier by Aeribacillus pallidus YM-1, J. Appl. Microbiol., 2012, vol. 113, pp. 44‒51.

    Article  CAS  PubMed  Google Scholar 

  67. Zhou, X., Xin, Z.J., Lu, X.H., Yang, X.P., Zhao, M.R., Wang, L., and Liang, J.P., High efficiency degradation crude oil by a novel mutant irradiated from Dietzia strain by 12C6+ heavy ion using response surface methodology, Bioresour. Technol., 2013, vol. 137, pp. 386‒393.

    Article  CAS  PubMed  Google Scholar 

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Solyanikova, I.P., Golovleva, L.A. Hexadecane and Hexadecane-Degrading Bacteria: Mechanisms of Interaction. Microbiology 88, 15–26 (2019). https://doi.org/10.1134/S0026261718060152

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