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An Update on the Genomic View of Mycobacterial High-Molecular-Weight Polycyclic Aromatic Hydrocarbon Degradation

  • Ohgew Kweon
  • Seong-Jae Kim
  • Carl E. CernigliaEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Bacteria play an important role in the degradation of high-molecular-weight (HMW) polycyclic aromatic hydrocarbons (PAHs), which are recalcitrant in the environment and potentially toxic to living organisms. A phylogenetically diverse bacterial community has been identified and characterized from PAH-contaminated soils and sediments that have the ability to degrade these ubiquitous pollutants. Strains of mycobacteria have frequently been found to degrade HMW PAHs. There are significant differences between the genetic systems in mycobacteria and other bacterial strains that degrade monocyclic aromatic compounds, low-molecular-weight (LMW), and HMW PAHs. Recently, a series of interdisciplinary studies using systems biology and analytical chemistry approaches has provided global insights into the structure, behavior, and evolution of mycobacterial HMW PAH degradation. In this review, we provide an update on genome-based systematic research with explanations and insights on the mycobacterial degradation of HMW PAHs.

Notes

Disclaimer

The views presented in this report are not necessarily those of the FDA.

References

  1. Andreoni V, Gianfreda L (2007) Bioremediation and monitoring of aromatic-polluted habitats. Appl Microbiol Biotechnol 76(2):287–308PubMedGoogle Scholar
  2. Assinder SJ, Williams PA (1990) The TOL plasmids: determinants of the catabolism of toluene and the xylenes. Adv Microb Physiol 31:1–69PubMedGoogle Scholar
  3. Badejo AC, Badejo AO, Shin KH, Chai YG (2013) A gene expression study of the activities of aromatic ring-cleavage dioxygenases in Mycobacterium gilvum PYR-GCK to changes in salinity and pH during pyrene degradation. PLoS One 8(2):e58066PubMedPubMedCentralGoogle Scholar
  4. Bastiaens L, Springael D, Wattiau P, Harms H, deWachter R, Verachtert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 66(5):1834–1843PubMedPubMedCentralGoogle Scholar
  5. Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59(6):1927–1930PubMedPubMedCentralGoogle Scholar
  6. Brezna B, Khan AA, Cerniglia CE (2003) Molecular characterization of dioxygenases from polycyclic aromatic hydrocarbon-degrading Mycobacterium spp. FEMS Microbiol Lett 223(2):177–183PubMedGoogle Scholar
  7. Brezna B, Kweon O, Stingley RL, Freeman JP, Khan AA, Polek B, Jones RC, Cerniglia CE (2006) Molecular characterization of cytochrome P450 genes in the polycyclic aromatic hydrocarbon degrading Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 71(4):522–532PubMedGoogle Scholar
  8. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368Google Scholar
  9. Cerniglia CE (2003) Recent advances in the biodegradation of polycyclic aromatic hydrocarbons by Mycobacterium species. In: Šašek V (ed) The utilization of bioremediation to reduce soil contamination: problems and solutions. Kluwer, Dordrecht, pp 51–73Google Scholar
  10. Cerniglia CE, Sutherland JB (2006) Relative roles of bacteria and fungi in polycyclic aromatic hydrocarbon biodegradation and bioremediation of contaminated soils. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, New YorkGoogle Scholar
  11. Child R, Miller CD, Liang Y, Narasimham G, Chatterton J, Harrison P, Sims RC, Britt D, Anderson AJ (2007) Polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates: their association with plant roots. Appl Microbiol Biotechnol 75(3):655–663PubMedGoogle Scholar
  12. Churchill SA, Harper JP, Churchill PF (1999) Isolation and characterization of a Mycobacterium species capable of degrading three- and four-ring aromatic and aliphatic hydrocarbons. Appl Environ Microbiol 65(2):549–552PubMedPubMedCentralGoogle Scholar
  13. Das K, Mukherjee AK (2007) Differential utilization of pyrene as the sole source of carbon by Bacillus subtilis and Pseudomonas aeruginosa strains: role of biosurfactants in enhancing bioavailability. J Appl Microbiol 102(1):195–203PubMedGoogle Scholar
  14. Dean-Ross D, Cerniglia CE (1996) Degradation of pyrene by Mycobacterium flavescens. Appl Microbiol Biotechnol 46(3):307–312PubMedGoogle Scholar
  15. DeBruyn JM, Mead TJ, Sayler GS (2012) Horizontal transfer of PAH catabolism genes in Mycobacterium: evidence from comparative genomics and isolated pyrene-degrading bacteria. Environ Sci Technol 46(1):99–106PubMedGoogle Scholar
  16. Diaz E (2004) Bacterial degradation of aromatic pollutants: a paradigm of metabolic versatility. Int Microbiol 7(3):173–180PubMedGoogle Scholar
  17. Fredslund L, Sniegowski K, Wick LY, Jacobsen CS, De Mot R, Springael D (2008) Surface motility of polycyclic aromatic hydrocarbon (PAH)-degrading mycobacteria. Res Microbiol 159:255–262PubMedGoogle Scholar
  18. Fritzsche C (1994) Degradation of pyrene at low defined oxygen concentrations by a Mycobacterium sp. Appl Environ Microbiol 60(5):1687–1689PubMedPubMedCentralGoogle Scholar
  19. Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369PubMedPubMedCentralGoogle Scholar
  20. Gibson DT, Mahadevan V, Jerina DM, Yogi H, Yeh HJ (1975) Oxidation of the carcinogens benzo[a]pyrene and benz[a]anthracene to dihydrodiols by a bacterium. Science 189(4199):295–297PubMedGoogle Scholar
  21. Grosser RJ, Warshawsky D, Vestal JR (1991) Indigenous and enhanced mineralization of pyrene, benzo[a]pyrene, and carbazole in soils. Appl Environ Microbiol 57(12):3462–3469PubMedPubMedCentralGoogle Scholar
  22. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67(2):225–243PubMedGoogle Scholar
  23. Hall K, Miller CD, Sorensen DL, Anderson AJ, Sims RC (2005) Development of a catabolically significant genetic probe for polycyclic aromatic hydrocarbon-degrading mycobacteria in soil. Biodegradation 16(5):475–484PubMedGoogle Scholar
  24. Hamann C, Hegemann J, Hildebrandt A (1999) Detection of polycyclic aromatic hydrocarbon degradation genes in different soil bacteria by polymerase chain reaction and DNA hybridization. FEMS Microbiol Lett 173(1):255–263PubMedGoogle Scholar
  25. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1–3):1–15PubMedGoogle Scholar
  26. Heitkamp MA, Cerniglia CE (1988) Mineralization of polycyclic aromatic hydrocarbons by a bacterium isolated from sediment below an oil field. Appl Environ Microbiol 54(6):1612–1614PubMedPubMedCentralGoogle Scholar
  27. Heitkamp MA, Freeman JP, Miller DW, Cerniglia CE (1988) Pyrene degradation by a Mycobacterium sp.; identification of ring oxidation and ring fission products. Appl Environ Microbiol 54(10):2556–2565PubMedPubMedCentralGoogle Scholar
  28. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133(1):71–84Google Scholar
  29. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodet Biodeg 45:57–88Google Scholar
  30. Kallimanis A, Karabika E, Mavromatis K, Lapidus A, Labutti KM, Liolios K, Ivanova N, Goodwin L, Woyke T, Velentzas AD, Perisynakis A, Ouzounis CC, Kyrpides NC, Koukkou AI, Drainas C (2011) Complete genome sequence of Mycobacterium sp. strain (Spyr1) and reclassification to Mycobacterium gilvum Spyr1. Stand Genomic Sci 5(1):144–153PubMedPubMedCentralGoogle Scholar
  31. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182(8):2059–2067PubMedPubMedCentralGoogle Scholar
  32. Kanaly RA, Harayama S (2010) Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb Biotechnol 3(2):136–164PubMedPubMedCentralGoogle Scholar
  33. Kazunga C, Aitken MD (2000) Products from the incomplete metabolism of pyrene by polycyclic aromatic hydrocarbon-degrading bacteria. Appl Environ Microbiol 66(5):1917–1922PubMedPubMedCentralGoogle Scholar
  34. Kelley I, Cerniglia CE (1995) Degradation of a mixture of high-molecular-weight polycyclic aromatic hydrocarbons by a Mycobacterium strain, PYR-1. J Soil Contam 4:77–91Google Scholar
  35. Kelley I, Freeman JP, Cerniglia CE (1990) Identification of metabolites from degradation of naphthalene by a Mycobacterium sp. Biodegradation 1(4):283–290PubMedGoogle Scholar
  36. Khan AA, Wang RF, Cao WW, Doerge DR, Wennerstrom D, Cerniglia CE (2001) Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1. Appl Environ Microbiol 67(8):3577–3585PubMedPubMedCentralGoogle Scholar
  37. Kim YH, Engesser KH, Cerniglia CE (2003) Two polycyclic aromatic hydrocarbon o-quinone reductases from a pyrene-degrading Mycobacterium. Arch Biochem Biophys 416:209–217PubMedGoogle Scholar
  38. Kim SJ, Kweon O, Freeman JP, Jones RC, Adjei MD, Jhoo JW, Edmondson RD, Cerniglia CE (2006) Molecular cloning and expression of genes encoding a novel dioxygenase involved in low- and high-molecular-weight polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 72(2):1045–1054PubMedPubMedCentralGoogle Scholar
  39. Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia CE (2007) Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol 189(2):464–472PubMedGoogle Scholar
  40. Kim S-J, Kweon O, Jones RC, Edmondson RD, Cerniglia CE (2008) Genomic analysis of polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Biodegradation 19(6):859–881PubMedGoogle Scholar
  41. Kim S-J, Kweon O, Cerniglia CE (2009) Proteomic applications to elucidate bacterial aromatic hydrocarbon metabolic pathways. Curr Opin Microbiol 12(3):301–309PubMedGoogle Scholar
  42. Kim S-J, Song J, Kweon O, Holland RD, Kim D-W, Kim J, Yu L-R, Cerniglia CE (2012) Functional robustness of a polycyclic aromatic hydrocarbon metabolic network examined in a nidA aromatic ring-hydroxylating oxygenase mutant of Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 78(10):3715–3723PubMedPubMedCentralGoogle Scholar
  43. Kim S-J, Kweon O, Sutherland JB, Kim H-L, Jones RC, Burback BL, Graves SW, Psurny E, Cerniglia CE (2015) Dynamic response of Mycobacterium vanbaalenii PYR-1 to BP Deepwater horizon crude oil. Appl Environ Microbiol 81(13):4263–4276PubMedPubMedCentralGoogle Scholar
  44. Krivobok S, Kuony S, Meyer C, Louwagie M, Willison JC, Jouanneau Y (2003) Identification of pyrene-induced proteins in Mycobacterium sp. strain 6PY1: evidence for two ring-hydroxylating dioxygenases. J Bacteriol 185(13):3828–3841PubMedPubMedCentralGoogle Scholar
  45. Kweon O, Kim SJ, Jones RC, Freeman JP, Adjei MD, Edmondson RD, Cerniglia CE (2007) A polyomic approach to elucidate the fluoranthene degradative pathway in Mycobacterium vanbaalenii PYR-1. J Bacteriol 189(13):4635–4647PubMedPubMedCentralGoogle Scholar
  46. Kweon O, Kim S-J, Freeman JP, Song J, Baek S, Cerniglia CE (2010) Substrate specificity and structural characteristics of the novel Rieske nonheme iron aromatic ring-hydroxylating oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1. MBio 1(2):e00135-10PubMedPubMedCentralGoogle Scholar
  47. Kweon O, Kim S-J, Holland RD, Chen H, Kim D-W, Gao Y, Yu L-R, Baek S, Baek D-H, Ahn H, Cerniglia CE (2011) Polycyclic aromatic hydrocarbon metabolic network in Mycobacterium vanbaalenii PYR-1. J Bacteriol 193(17):4326–4337PubMedPubMedCentralGoogle Scholar
  48. Kweon O, Kim S-J, Kim D-W, Kim JM, Kim H-l, Ahn Y, Sutherland JB, Cerniglia CE (2014) Pleiotropic and epistatic behavior of a ring-hydroxylating oxygenase system in the polycyclic aromatic hydrocarbon metabolic network from Mycobacterium vanbaalenii PYR-1. J Bacteriol 196(19):3503–3515PubMedPubMedCentralGoogle Scholar
  49. Kweon O, Kim S-J, Blom J, Kim S-K, Kim B-S, Baek D-H, Park SI, Sutherland JB, Cerniglia CE (2015) Comparative functional pan-genome analyses to build connections between genomic dynamics and phenotypic evolution in polycyclic aromatic hydrocarbon metabolism in the genus Mycobacterium. BMC Evol Biol 15:21PubMedPubMedCentralGoogle Scholar
  50. Kweon O, Kim S-J, Sutherland JB, Cerniglia CE (2016) Novel insights into polycyclic aromatic hydrocarbon biodegradatin pathways using systems biology and bioinformatics approaches. In: Długoński J (ed) Microbial biodegradation: from omics to function and application. Caister Academic Press, Norfolk, pp 143–166Google Scholar
  51. López Z, Vila J, Grifoll M (2005) Metabolism of fluoranthene by mycobacterial strains isolated by their ability to grow in fluoranthene or pyrene. J Ind Microbiol Biotechnol 32(10):455–464PubMedGoogle Scholar
  52. Miller CD, Hall K, Liang YN, Nieman K, Sorensen D, Issa B, Anderson AJ, Sims RC (2004) Isolation and characterization of polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates from soil. Microb Ecol 48(2):230–238PubMedGoogle Scholar
  53. Moody JD, Freeman JP, Fu PP, Cerniglia CE (2004) Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 70:340–345PubMedPubMedCentralGoogle Scholar
  54. Pagnout C, Frache G, Poupin P, Maunit B, Muller JF, Ferard JF (2007) Isolation and characterization of a gene cluster involved in PAH degradation in Mycobacterium sp. strain SNP11: expression in Mycobacterium smegmatis mc2155. Res Microbiol 158(2):175–186PubMedGoogle Scholar
  55. Pazos F, Valencia A, De Lorenzo V (2003) The organization of the microbial biodegradation network from a systems-biology perspective. EMBO Rep 4(10):994–999PubMedPubMedCentralGoogle Scholar
  56. Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32(6):927–955PubMedGoogle Scholar
  57. Pinyakong O, Habe H, Omori T (2003) The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). J Gen Appl Microbiol 49(1):1–19PubMedGoogle Scholar
  58. van der Meer JR, de Vos WM, Harayama S, Zehnder AJ (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev 56(4):677–694PubMedPubMedCentralGoogle Scholar
  59. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67(4):503–549PubMedPubMedCentralGoogle Scholar
  60. Vila J, López Z, Sabaté J, Minguillón C, Solanas AM, Grifoll M (2001) Identification of a novel metabolite in the degradation of pyrene by Mycobacterium sp. strain AP1: actions of the isolate on two- and three-ring polycyclic aromatic hydrocarbons. Appl Environ Microbiol 67(12):5497–5505PubMedPubMedCentralGoogle Scholar
  61. Walter U, Beyer M, Klein J, Rehm HJ (1991) Degradation of pyrene by Rhodococcus sp. UW1. Appl Microbiol Biotechnol 34:671–676Google Scholar
  62. Wick LY, Ruiz de Munain A, Springael D, Harms H, de MA (2002) Responses of Mycobacterium sp. LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58(3):378–385PubMedGoogle Scholar
  63. Wick LY, Pelz O, Bernasconi SM, Andersen N, Harms H (2003) Influence of the growth substrate on ester-linked phospho- and glycolipid fatty acids of PAH-degrading Mycobacterium sp. LB501T. Environ Microbiol 5(8):672–680PubMedGoogle Scholar
  64. Williams PA, Sayers JR (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas. Biodegradation 5(3–4):195–217PubMedGoogle Scholar
  65. Zhao JK, Li XM, Ai GM, Deng Y, Liu SJ, Jiang CY (2016) Reconstruction of metabolic networks in a fluoranthene-degrading enrichments from polycyclic aromatic hydrocarbon polluted soil. J Hazard Mater 318:90–98PubMedGoogle Scholar
  66. Zhou HW, Guo CL, Wong YS, Tam NF (2006) Genetic diversity of dioxygenase genes in polycyclic aromatic hydrocarbon-degrading bacteria isolated from mangrove sediments. FEMS Microbiol Lett 262(2):148–157PubMedGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  • Ohgew Kweon
    • 1
  • Seong-Jae Kim
    • 1
  • Carl E. Cerniglia
    • 1
    Email author
  1. 1.Division of MicrobiologyNational Center for Toxicological Research, Food and Drug AdministrationJeffersonUSA

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