Insights into the anaerobic biodegradation pathway of n-Alkanes in oil reservoirs by detection of signature metabolites

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bian, Xin Yu ^a,b   Mbadinga, Serge Maurice ^a,b   Liu, Yi Fan ^a,b   Yang, Shi Zhong ^a,b   Liu, Jin Feng ^a,b   Ye, Ru Qiang ^a,b   Gu, Ji Dong ^c   Mu, Bo Zhong ^a,b  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b SHANGHAI COLLABORATIVE INNOVATION CENTER FOR BIOMANUFACTURING TECHNOLOGY   (China)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ALKANE; BACTERIAL DNA; PETROLEUM;

ANAEROBIC BACTERIUM; BIOREMEDIATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ALKANES; BACTERIA, ANAEROBIC; BASE SEQUENCE; BIODEGRADATION, ENVIRONMENTAL; DNA, BACTERIAL; MOLECULAR SEQUENCE DATA; PETROLEUM;

EID: 84929353273     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09801     Document Type: Article

References (60)

1. Labinger, J. A. & Bercaw, J. E. Understanding and exploiting C-H bond activation. Nature 417, 507-514 (2002).
2. Mbadinga, S. M. et al. Microbial communities involved in anaerobic degradation of alkanes. Int. Biodeter. Biodegr. 65, 1-13 (2011).
3. Heider, J. & Schuhle, K. [Anaerobic biodegradation of hydrocarbons including methane] The Prokaryotes [Rosenberg E.(ed.)] [1028-1049] (Springer, Berlin Heidelberg, 2013).
4. Singh, S., Kumari, B. & Mishra, S. [Microbial degradation of alkanes] Microbial Degradation of Xenobiotics [Singh S. N. (ed)] [439-469] (Springer, Berlin Heidelberg, 2012).
5. Widdel, F., Knittel, K. & Galushko, A. [Anaerobic hydrocarbon-degrading microorganisms: an overview] Handbook of hydrocarbon and lipid microbiology [Timmis K. N. (ed.)] [1997-2021] (Springer, Berlin Heidelberg, 2010).
6. Grossi, V., Cravo-Laureau, C., Guyoneaud, R., Ranchou-Peyruse, A. & Hirschler-Rea, A. Metabolism of n-alkanes and n-alkenes by anaerobic bacteria: A summary. Org. Geochem. 39, 1197-1203 (2008).
7. Das, N. & Chandran, P. Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotech. Res. Int. 2011, Article ID 941810, doi:10.4061/2011/941810 (2010).
8. Head, I. M., Jones, D. M. & Larter, S. R. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426, 344-352 (2003).
9. Aitken, C. M., Jones, D. M. & Larter, S. R. Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature 431, 291-294 (2004).
10. Jones, D. M. et al. Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451, 176-180 (2007).
11. Magot, M., Ollivier, B. & Patel, B. K. Microbiology of petroleum reservoirs. A. Van. Leeuw. 77, 103-116 (2000).
12. Mbadinga, S. M. et al. Analysis of alkane-dependent methanogenic community derived from production water of a hightemperature petroleum reservoir. Appl. Microbiol. Biotechnol. 96, 531-542 (2012).
13. Li, W. et al. Microbial community characteristics of petroleum reservoir production water amended with n-alkanes and incubated under nitrate-, sulfate-reducing and methanogenic conditions. Int. Biodeter. Biodegr. 69, 87-96 (2012).
14. Zhou, L. et al. Analyses of n-alkanes degrading community dynamics of a high-temperature methanogenic consortium enriched from production water of a petroleum reservoir by a combination of molecular techniques. Ecotoxicology 21, 1680-1691 (2012).
15. Berdugo-Clavijo, C. & Gieg, L. Conversion of crude oil to methane by a microbial consortium enriched from oil reservoir production waters. Front. Microbiol. 5, 197, doi:10.3389/fmicb.2014.00197 (2014).
16. Hasegawa, R., Toyama, K., Miyanaga, K. & Tanji, Y. Identification of crude-oil components and microorganisms that cause souring under anaerobic conditions. Appl. Microbiol. Biotechnol. 98, 1853-1861 (2014).
17. Gieg, L. M., Davidova, I. A., Duncan, K. E. & Suflita, J. M. Methanogenesis, sulfate reduction and crude oil biodegradation in hot Alaskan oilfields. Environ. Microbiol. 12, 3074-3086 (2010).
18. Aitken, C. M. et al. Evidence that crude oil alkane activation proceeds by different mechanisms under sulfate-reducing and methanogenic conditions. Geochim. Cosmochim. Ac. 109, 162-174 (2013).
19. Agrawal, A. & Gieg, L. M. In situ detection of anaerobic alkane metabolites in subsurface environments. Front. Microbiol. 4, 140, doi:10.3389/fmicb.2013.00140 (2013).
20. Callaghan, A. V. Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front. Microbiol. 4, 89, doi:10.3389/fmicb.2013.00089 (2013).
21. Wilkes, H. et al. Anaerobic degradation of n-hexane in a denitrifying bacterium: Further degradation of the initial intermediate (1-methylpentyl)succinate via C-skeleton rearrangement. Arch. Microbiol. 177, 235-243 (2002).
22. Grundmann, O. et al. Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN1. Environ. Microbiol. 10, 376-385 (2008).
23. Callaghan, A. V., Wawrik, B., Ni Chadhain, S. M., Young, L. Y. & Zylstra, G. J. Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes. Biochem. Bioph. Res. Co. 366, 142-148 (2008).
24. Callaghan, A. V., Gieg, L. M., Kropp, K. G., Suflita, J. M. & Young, L. Y. Comparison of mechanisms of alkane metabolism under sulfate-reducing conditions among two bacterial isolates and a bacterial consortium. Appl. Environ. Microb. 72, 4274-4282 (2006).
25. Rabus, R. et al. Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J. Bacteriol. 183, 1707-1715 (2001).
26. Wilkes, H. et al. Formation of n-alkane-and cycloalkane-derived organic acids during anaerobic growth of a denitrifying bacterium with crude oil. Org. Geochem. 34, 1313-1323 (2003).
27. Cravo-Laureau, C., Grossi, V., Raphel, D., Matheron, R. & Hirschler-Rea, A. Anaerobic n-alkane metabolism by a sulfatereducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T. Appl. Environ. Microb. 71, 3458 (2005).
28. Davidova, I. A., Gieg, L. M., Nanny, M., Kropp, K. G. & Suflita, J. M. Stable isotopic studies of n-alkane metabolism by a sulfatereducing bacterial enrichment culture. Appl. Environ. Microb. 71, 8174-8182 (2005).
29. Musat, F., Wilkes, H., Behrends, A., Woebken, D. & Widdel, F. Microbial nitrate-dependent cyclohexane degradation coupled with anaerobic ammonium oxidation. ISME J. 4, 1290-1301 (2010).
30. Kropp, K. G., Davidova, I. A. & Suflita, J. M. Anaerobic oxidation of n-dodecane by an addition reaction in a sulfate-reducing bacterial enrichment culture. Appl. Environ. Microb. 66, 5393-5398 (2000).
31. Kniemeyer, O. et al. Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449, 898-901 (2007).
32. Rios-Hernandez, L. A., Gieg, L. M. & Suflita, J. M. Biodegradation of an alicyclic hydrocarbon by a sulfate-reducing enrichment from a gas condensate-contaminated aquifer. Appl. Environ. Microb. 69, 434-443 (2003).
33. Widdel, F. & Rabus, R. Anaerobic biodegradation of saturated and aromatic hydrocarbons Curr. Opin. Biotech. 12, 259-276 (2001).
34. Meckenstock, R. U., Safinowski, M. & Griebler, C. Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol. Ecol. 49, 27-36 (2004).
35. Biegert, T., Fuchs, G. & Heider, J. Evidence that anaerobic oxidation of toluene in the denitrifying bacterium thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur. J. Biochem. 238, 661-668 (1996).
36. Gieg, L. M. et al. Assessing in situ rates of anaerobic hydrocarbon bioremediation. Microb. Biotech. 2, 222-233 (2009).
37. Callaghan, A. V. Metabolomic investigations of anaerobic hydrocarbon-impacted environments. Curr. Opin. Biotech. 24, 506-515 (2013).
38. Gieg, L. M. & Suflita, J. M. Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ. Sci. Technol. 36, 3755-3762 (2002).
39. Parisi, V. A. et al. Field metabolomics and laboratory assessments of anaerobic intrinsic bioremediation of hydrocarbons at a petroleum-contaminated site. Microb. Biotech. 2, 202-212 (2009).
40. Callaghan, A. V. et al. Diversity of benzyl-and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. Environ. Sci. Technol. 44, 7287-7294 (2010).
41. von Netzer, F. et al. Enhanced gene detection assays for fumarate-adding enzymes allow uncovering of anaerobic hydrocarbon degraders in terrestrial and marine systems. Appl. Environ. Microb. 79, 543-552 (2013).
42. Kimes, N. E. et al. Metagenomic analysis and metabolite profiling of deep-sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill. Front. Microbiol. 4, 50, doi:10.3389/fmicb.2013.00050 (2013).
43. Duncan, K. E. et al. Biocorrosive thermophilic microbial communities in Alaskan North Slope oil facilities. Environ. Sci. Technol. 43, 7977-7984 (2009).
44. Bian, X.-Y. et al. Synthesis of anaerobic degradation biomarkers alkyl-, aryl-and cycloalkylsuccinic acids and their mass spectral characteristics. Eur. J. Mass Spectrom 20, 287-297 (2014).
45. Tierney, M. & Young, L. [Anaerobic degradation of aromatic hydrocarbons] Handbook of Hydrocarbon and Lipid Microbiology [Timmis K. N. (ed.)] [925-934] (Springer, Berlin Heidelberg, 2010).
46. Embree, M., Nagarajan, H., Movahedi, N., Chitsaz, H. & Zengler, K. Single-cell genome and metatranscriptome sequencing reveal metabolic interactions of an alkane-degrading methanogenic community. ISME J. 8, 757-767 (2014).
47. Tan, B., Nesbo, C. & Foght, J. Re-analysis of omics data indicates Smithella may degrade alkanes by addition to fumarate under methanogenic conditions. ISME J. 8, 2353-2356 (2014).
48. Aktas, D. F. et al. Effects of oxygen on biodegradation of fuels in a corroding environment. Int. Biodeter. Biodegr. 81, 114-126 (2013).
49. Kleindienst, S. et al. Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J. 8, 2029-2044 (2014).
50. Gray, N. D., Sherry, A., Hubert, C., Dolfing, J. & Head, I. M. Methanogenic degradation of petroleum hydrocarbons in subsurface environments: remediation, heavy oil formation, and energy recovery. Adv. Appl. Microbiol. 72, 137-161 (2010).
51. Jones, D. M. et al. Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451, 176-180 (2008).
52. Sherry, A. et al. Volatile hydrocarbons inhibit methanogenic crude oil degradation. Front. Microbiol. 5, 131, doi:10.3389/ fmicb.2014.00131 (2014).
53. Boll, M., Fuchs, G. & Heider, J. Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr. Opin. Chem. Biol. 6, 604-611 (2002).
54. Gray, N. et al. The quantitative significance of Syntrophaceae and syntrophic partnerships in methanogenic degradation of crude oil alkanes. Environ. Microbiol. 13, 2957-2975 (2011).
55. Liu, Y., Balkwill, D. L., Aldrich, H. C., Drake, G. R. & Boone, D. R. Characterization of the anaerobic propionate-degrading syntrophs Smithella propionica gen. nov., sp. nov. and Syntrophobacter wolinii. Int. J. Syst. Bacteriol. 49, 545-556 (1999).
56. Wang, L. Y. et al. Methanogenic microbial community composition of oily sludge and its enrichment amended with alkanes incubated for over 500 days. Geomicrobiol. J. 29, 716-726 (2012).
57. Weckwerth, W. Metabolomics in systems biology. Annu. Rev. Plant. Biol. 54, 669-689 (2003).
58. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539-544 (2011).
59. Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
60. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013).