Diversity of metabolically active bacteria in water-flooded high-temperature heavy oil reservoir

Frontiers in Microbiology

Volumn 8, Issue APR, 2017, Pages

  Nazina, Tamara N ^a   Shestakova, Natalya M ^a   Semenova, Ekaterina M ^a   Korshunova, Alena V ^a   Kostrukova, Nadezda K ^a   Tourova, Tatiana P ^a   Min, Liu ^b   Feng, Qingxian ^b   Poltaraus, Andrey B ^c  

^a WINOGRADSKY INSTITUTE OF MICROBIOLOGY   (Russian Federation)

^b PETROCHINA DAGANG OILFIELD COMPANY   (China)

^c ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

16S rRNA gene clone library; Biogeochemical processes and cycles; CDNA of 16S rRNA; Gene alkB; Metabolic activity; Near bottom zone of injection well; Petroleum reservoir

Indexed keywords

ALKB PROTEIN; CARBON; COMPLEMENTARY DNA; RADIOISOTOPE; RNA 16S; TRACER; WATER;

ARCHAEON; ARTICLE; BACTERIUM; BIOGEOCHEMICAL CYCLE; CELL COUNTING; DNA EXTRACTION; FOOD CHAIN; GENETIC VARIABILITY; GEOBACILLUS; GEOCHEMICAL ANALYSIS; HIGH TEMPERATURE; METHANOGENESIS; METHANOGENIC BACTERIUM; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MICROBIAL DIVERSITY; MOLECULAR CLONING; MOLECULAR LIBRARY; NONHUMAN; NUCLEOTIDE SEQUENCE; OIL FIELD; PHYLOGENETIC TREE; PHYSICAL CHEMISTRY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEQUENCE ANALYSIS;

EID: 85018367248     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00707     Document Type: Article

References (71)

1. Acinas, S. G., Marcelino, L. A., Klepac-Ceraj, V., and Polz, M. F. (2004). Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186, 2629-2635. doi: 10.1128/JB.186.9.2629-2635.2004
2. An, D., Caffrey, S. M., Soh, J., Agrawal, A., Brown, D., et al. (2013). Metagenomics of hydrocarbon resource environments indicates aerobic taxa and genes to be unexpectedly common. Environ. Sci. Technol. 47, 10708-10717. doi: 10.1021/es4020184
3. Belyaev, S. S., Laurinavichus, K. S., Obraztsova, A. Y., Gorlatov, S. N., and Ivanov, M. V. (1982). Microbiological processes in the critical zone of injection wells. Microbiology (Moscow). 51, 997-1001
4. Blazewicz, S. J., Barnard, R. L., Daly, R. A., and Firestone, M. K. (2013). Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 7, 2061-2068. doi: 10.1038/ismej.2013.102
5. Bødtker, G., Lysnes, K., Torsvik, T., Bjørnestad, E. Ø., and Sunde, E. (2009). Microbial analysis of backflowed injection water from a nitrate-treated North Sea oil reservoir. J. Ind. Microbiol. Biotechnol. 36, 439-450. doi: 10.1007/s10295-008-0515-6
6. Bonch-Osmolovskaya, E. A., Miroshnichenko, M. L., Lebedinsky, A. V., Chernyh, N. A., Nazina, T. N., Ivoilov, V. S., et al. (2003). Radioisotopic, culture-based, and oligonucleotide microchip analyses of thermophilic microbial communities in a continental high-temperature petroleum reservoir. Appl. Environ. Microbiol. 69, 6143-6151. doi: 10.1128/AEM.69.10.6143-6151.2003
7. Brunk, C. F., Avaniss-Aghajani, E., and Brunk, C. A. (1996). A computer analysis of primer and probe hybridization potential with bacterial small-subunit rRNA sequences. Appl. Environ. Microbiol. 61, 872-879
8. Cai, M., Chan, Yu, C., Wang, R., Si, Y., Masakorala, K., Yuan, H., et al. (2015). Effects of oxygen injection on oil biodegradation and biodiversity of reservoir microorganisms in Dagang oil field, China. Int. Biodeter. Biodeg. 98, 59-65. doi: 10.1016/j.ibiod.2014.12.003
9. Chen, W. M., Huang, H. W., Chang, J. S., Han, Y. L., Guo, T. R., and Sheu, S. Y. (2013). Tepidimonas fonticaldi sp. nov., a slightly thermophilic betaproteobacterium isolated from a hot spring. Int. J. Syst. Evol. Microbiol. 63, 1810-1816. doi: 10.1099/ijs.0.043729-0
10. Craig, H. (1953). The geochemistry of the stable carbon isotopes. Geochim. Cosmochim. Acta 3, 53-92. doi: 10.1016/0016-7037(53)90001-5
11. Dojka, M. A., Hugenholtz, P., Haack, S. K., and Pace, N. R. (1998). Microbial diversity in a hydrocarbon-and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64, 3869-3877
12. Duncan, K. E., Gieg, L. M., Parisi, V. A., Tanner, R. S., Suflita, J. M., Green Tringe, S., et al. (2009). Biocorrosive thermophilic microbial communities in Alaskan North Slope oil facilities. Environ. Sci. Technol. 43, 7977-7984. doi: 10.1021/es9013932
13. Feng, W.-W., Liu, J.-F., Gu, J.-D., and Mu, B.-Z. (2011). Nitrate-reducing community in production water of three oil reservoirs and their responses to different carbon sources revealed by nitrate-reductase encoding gene (napA). Int. Biodeter. Biodeg. 65, 1081-1086. doi: 10.1016/j.ibiod.2011.05.009
14. Gao, P. K., Li, G. Q., Tian, H. M., Wang, Y. S., Sun, H. W., and Ma, T. (2015). Differences in microbial community composition between injection and production water samples of water flooding petroleum reservoirs. Biogeosciences 12, 3403-3414. doi: 10.5194/bg-12-3403-2015
15. Gieg, L. M., Davidova, I. A., Duncan, K. E., and Suflita, J. M. (2010). Methanogenesis, sulfate reduction and crude oil biodegradation in hot Alaskan oilfields. Environ. Microbiol. 12, 3074-3086. doi: 10.1111/j.1462-2920.2010.02282.x
16. Gieg, L. M., Duncan, K. E., and Suflita, J. M. (2008). Bioenergy production via microbial conversion of residual oil to natural gas. Appl. Environ. Microbiol. 74, 3022-3029. doi: 10.1128/AEM.00119-08
17. Gittel, A., Sorensen, K. B., Skovhus, T. L., Ingvorsen, K., and Schramm, A. (2009). Prokaryotic community structure and activity of sulfate reducers in production water from high-temperature oil reservoirs with and without nitrate treatment. Appl. Environ. Microbiol. 75, 7086-7096. doi: 10.1128/AEM.01123-09
18. Good, I. J. (1953). The population frequencies of species and the estimation of population parameters. Biometrika 40, 237-264. doi: 10.1093/biomet/40.3-4.237
19. Gray, N. D., Sherry, A., Hubert, C., Dolfing, J., and Head, I. M. (2010). Methanogenic degradation of petroleum hydrocarbons in subsurface environments remediation, heavy oil formation, and energy recovery. Adv. Appl. Microbiol. 72, 137-161. doi: 10.1016/S0065-2164(10)72005-0
20. Head, I. M., Gray, N. D., and Larter, S. R. (2014). Life in the slow lane; biogeochemistry of biodegraded petroleum containing reservoirs and implications for energy recovery and carbon management. Front. Microbiol. 5:566. doi: 10.3389/fmicb.2014.00566
21. Heck, K. L. Jr., van Belle, G., and Simberloff, D. (1975). Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56, 1459-1461. doi: 10.2307/1934716
22. Iino, T., Nakagawa, T., Mori, K., Harayama, S., and Suzuki, K. (2008). Calditerrivibrio nitroreducens gen. nov., sp. nov., a thermophilic, nitrate-reducing bacterium isolated from a terrestrial hot spring in Japan. Int. J. Syst. Evol. Microbiol. 58, 1675-1679. doi: 10.1099/ijs.0.65714-0
23. Jiménez, N., Morris, B. E. L., Cai, M., Gründger, F., Yao, J., Richnow, H. H., et al. (2012). Evidence for in situ methanogenic oil degradation in the Dagang oil field. Org. Geochem. 52, 44-54. doi: 10.1016/j.orggeochem.2012.08.009
24. Jones, D. M., Head, I. M., Gray, N. D., Adams, J. J., Rowan, A., Aitken, C., et al. (2008). Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451, 176-180. doi: 10.1038/nature06484
25. Kato, T., Haruki, M., Imanaka, T., Morikawa, M., and Kanaya, S. (2001). Isolation and characterization of psychrotrophic bacteria from oil-reservoir water and oil sands. Appl. Microbiol. Biotechnol. 55, 794-800. doi: 10.1007/s002530000556
26. Kolganova, T. V., Kuznetsov, B. B., and Turova, T. P. (2002). Selection and testing of oligonucleotide primers for amplification sequencing of archaeal 16S rRNA genes. Microbiology (Moscow). 71, 283-285. doi: 10.1023/A:1015122926687
27. Kuznetsov, S. I., Ivanov, M. V., and Lyalikova, N. N. (1963). Introduction in Geological Microbiology (English translation), ed C. H. Oppenheimer. New York, NY: McGraw-Hill
28. Kuznetsova, V. A., and Li, A. D. (1964). Development of sulphate reducing bacteria in oil-bearing beds D1 of the flooded Romashkino field. Microbiology 33, 314-320
29. L'Haridon, S., Miroshnichenko, M. L., Hippe, H., Fardeau, M. L., Bonch-Osmolovskaya, E., Stackebrandt, E., et al. (2001). Thermosipho geolei sp. nov., a thermophilic bacterium isolated from a continental petroleum reservoir in Western Siberia. Int. J. Syst. Evol. Microbiol. 51, 1327-1334. doi: 10.1099/00207713-51-4-1327
30. Liang, B., Wang, L.-Y., Mbadinga, S. M., Liu, J.-F., Yang, S.-Z., Gu, J.-D., et al. (2015). Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation. AMB Express. 5, 37. doi: 10.1186/s13568-015-0117-4
31. Magot, M., Ollivier, B., and Patel, B. K. C. (2000). Microbiology of petroleum reservoirs. Antonie van Leeuwenhoek. 77, 103-116. doi: 10.1023/A:1002434330514
32. McKinley, V. L., Costerton, J. W., and White, D. C. (1988). Microbial biomass, activity, and community structure of water and particulates retrieved by backflow from a waterflood injection well. Appl. Environ. Microbiol. 54, 1383-1393
33. Mills, H. J., Martinez, R. J., Story, S., and Sobecky, P. A. (2005). Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA-and RNA-derived clone libraries. Appl. Environ. Microbiol. 71, 3235-3247. doi: 10.1128/AEM.71.6.3235-3247.2005
34. Mills, H. J., Reese, B. K., Shepard, A. K., Riedinger, N., Dowd, S. E., Morono, Y., et al. (2012). Characterization of metabolically active bacterial populations in subseafloor Nankai Trough sediments above, within, and below the sulfate-methane transition zone. Front. Microbio. 3:113. doi: 10.3389/fmicb.2012.00113
35. Moeseneder, M. M., Arrieta, J. M., and Herndl, G. H. (2005). A comparison of DNA-and RNA-based clone libraries from the same marine bacterioplankton community. FEMS Microbiol. Ecol. 51, 341-352. doi: 10.1016/j.femsec.2004.09.012
36. Mori, K., and Suzuki, K. (2008). Thiofaba tepidiphila gen. nov., sp. nov., a novel obligately chemolithoautotrophic, sulfur-oxidizing bacterium of the Gammaproteobacteria isolated from a hot spring. Int. J. Syst. Evol. Microbiol. 58, 1885-1891. doi: 10.1099/ijs.0.65754-0
37. Nazina, T. N., Grigor'yan, A. A., Shestakova, N. M., Babich, T. L., Ivoilov, V. S., Feng, Q., et al. (2007a). Microbiological investigations of high-temperature horizons of the Kongdian petroleum reservoir in connection with field trial of a biotechnology for enhancement of oil recovery. Microbiology 76, 287-296. doi: 10.1134/S0026261707030058
38. Nazina, T. N., Grigor'yan, A. A., Feng, Q., Shestakova, N. M., Babich, T. L., Pavlova, N. K., et al. (2007b). Microbiological and production characteristics of the high-temperature Kongdian petroleum reservoir revealed during field trial of biotechnology for the enhancement of oil recovery. Microbiology 76, 297-309. doi: 10.1134/S002626170703006X
39. Nazina, T. N., Grigor'yan, A. A., Shestakova, N. M., Babich, T. L., Pavlova, N. K., Ivoilov, V. S., et al. (2008). MEOR study enhances production in a high-temperature reservoir. World Oil June, 97-101
40. Nazina, T. N., Ivanova, A. E., Borzenkov, I. A., Belyaev, S. S., and Ivanov, M. V. (1995). Occurrence and geochemical activity of microorganisms in high-temperature water-flooded oil fields of Kazakhstan and Western Siberia. Geomicrobiol. J. 13, 181-192. doi: 10.1080/01490459509378016
41. Nazina, T. N., Rozanova, E. P., and Kuznetsov, S. I. (1985). Microbial oil transformation processes accompanied by methane and hydrogen-sulfide formation. Geomicrobiol. J. 4, 103-130. doi: 10.1080/01490458509385927
42. Nazina, T. N., Shestakova, N. M., Grigor'yan, A. A., Mikhailova, E. M., Tourova, T. P., Poltaraus, A. B., et al. (2006). Phylogenetic diversity and activity of anaerobic microorganisms of high-temperature horizons of the Dagang oil field (P. R. China). Microbiology 75, 55-65. doi: 10.1134/S0026261706010115
43. Nazina, T. N., Sokolova, D., Sh., Grigoryan, A. A., Shestakova, N. M., Mikhailova, E. M., Poltaraus, A. B., et al. (2005). Geobacillus jurassicus sp. nov., a new thermophilic bacterium isolated from a high-temperature petroleum reservoir, and the validation of the Geobacillus species. Syst. Appl. Microbiol. 28, 43-53. doi: 10.1016/j.syapm.2004.09.001
44. Neef, A., Arnann, R., Schlesner, H., and Schleifer, K.-H. (1998). Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144, 3257-3266. doi: 10.1099/00221287-144-12-3257
45. Nobu, M. K., Dodsworth, J. A., Murugapiran, S. K., Rinke, C., Gies, E. A., Webster, G., et al. (2016). Phylogeny and physiology of candidate phylum 'Atribacteria' (OP9/JS1) inferred from cultivation-independent genomics. ISME J. 10, 273-286. doi: 10.1038/ismej.2015.97
46. Orphan, V. J., Goffredi, S. K., Delong, E. F., and Boles, J. R. (2003). Geochemical influence on diversity and microbial processes in high-temperature oil reservoirs. Geomicrobiol. J. 20, 295-311. doi: 10.1080/01490450303898
47. Pelletier, E., Kreimeyer, A., Bocs, S., Rouy, Z., Gyapay, G., Chouari, R., et al. (2008). "Candidatus Cloacamonas acidaminovorans": genome sequence reconstruction provides a first glimpse of a new bacterial division. J. Bacteriol. 190, 2572-2579. doi: 10.1128/JB.01248-07
48. Podosokorskaya, O. A., Kadnikov, V. V., Gavrilov, S. N., Mardanov, A. V., Merkel, A. Y., Karnachuk, O. V., et al. (2013). Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ. Microbiol. 15, 1759-1771. doi: 10.1111/1462-2920.12067
49. Ren, H-Y., Zhang, X-J., Song, Z.-Y., Rupert, W., Gao, G-J., Guo, S.-X., et al. (2011). Comparison of microbial community compositions of injection and production well samples in a long-term water-flooded petroleum reservoir. PLoS ONE 6:e23258. doi: 10.1371/journal.pone.0023258
50. Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J. F., et al. (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437. doi: 10.1038/nature12352
51. Rozanova, E. P., and Nazina, T. N. (1982). Hydrocarbon-oxidizing bacteria and their activity in oil pools. Microbiology (Moscow). 51, 287-293
52. Rozanova, E. P., Savvichev, A. S., Karavaiko, S. G., and Miller, Y. M. (1995). Microbial processes in the Savuiskoe oil-field in the Ob region. Microbiology (Moscow). 64, 85-90
53. Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., et al. (2000). Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23, 93-106. doi: 10.1016/S0723-2020(00)80050-8
54. Shestakova, N. M., Ivoilov, V. S., Tourova, T. P., Belyaev, S. S., Poltaraus, A. B., and Nazina, T. N. (2011a). "Application of clone libraries: syntrophic acetate degradation to methane in a high-temperature petroleum reservoir: culture-based and 16S rRNA genes characterization," in Applied Microbiology and Molecular Biology in Oil Field Systems, eds C. Whitby and T. L. Skovhus (Dordrecht; Heidelberg; London; New York, NY: Springer), Chapter 6, 45-53. doi: 10.1007/978-90-481-9252-6_6
55. Shestakova, N. M., Korshunova, A. V., Mikhailova, E. M., Sokolova, D. Sh. Tourova, T. P., Belyaev, S. S., et al. (2011b). Characterization of the aerobic hydrocarbon-oxidizing enrichments from a high-temperature petroleum reservoir by comparative analysis of DNA-and RNA-derived clone libraries. Microbiology (Moscow). 80, 60-69. doi: 10.1134/S0026261711010140
56. Slobodkin, A. I., Jeanthon, C., L'Haridon, S., Nazina, T. N., Miroshnichenko, M. L., and Bonch-Osmolovskaya, E. A. (1999). Dissimilatory reduction of Fe(III) by thermophilic bacteria and archaea in deep subsurface petroleum reservoirs of Western Siberia. Curr. Microbiol. 39, 99-102. doi: 10.1007/s002849900426
57. Stetter, K. O., Huber, R., Blöchl, E., Kurr, M., Eden, R. D., Fielder, M., et al. (1993). Hyperthermophilic archaea are thriving in deep North Sea and Alaskan oil reservoirs. Nature 365, 743-745. doi: 10.1038/365743a0
58. Stoddard, S. F., Smith, B. J., Hein, R., Roller, B. R., and Schmidt, T. M. (2015). rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 43, D593-D598. doi: 10.1093/nar/gku1201
59. Takahata, Y., Nishijima, M., Hoaki, T., and Maruyama, T. (2000). Distribution and physiological characteristics of hyperthermophiles in the Kubiki oil reservoir in Niigata, Japan. Appl. Environ. Microbiol. 66, 73-79. doi: 10.1128/AEM.66.1.73-79.2000
60. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 9, 3251-3270. doi: 10.1093/nar/22.22.4673
61. Tourova, T. P., Nazina, T. N., Mikhailova, E. M., Rodionova, T. A., Ekimov, A. N., Mashukova, A. V., et al. (2008). alkB homologs in thermophilic bacteria of the genus Geobacillus. Molecular Biology. 42, 217-226. doi: 10.1134/S0026893308020076
62. Våge, S., and Thingstad, T. F. (2015). Fractal hypothesis of the pelagic microbial ecosystem-can simple ecological principles lead to self-similar complexity in the pelagic microbial food web? Front. Microbio. 6:1357. doi: 10.3389/fmicb.2015.01357
63. Van der Kraan, G. M., Bruining, J., Lomans, B. P., van Loosdrecht, M. C. M., and Muyzer, G. (2010). Microbial diversity of an oil-water processing site and its associated oilfield: the possible role of microorganisms as information carriers from oil-associated environments. FEMS Microbiol. Ecol. 71, 428-443. doi: 10.1111/j.1574-6941.2009.00813.x
64. Verde, L. C. L., e Silva, T. R., Dellagnezze, B. M., Santos Neto, E. V. D., and de Oliveira, V. M. (2013). Diversity of hydrocarbon-related catabolic genes in oil samples from Potiguar Basin (Rn, Brazil). J. Petrol. Environ. Biotechnol. 4:138. doi: 10.4172/2157-7463.1000138
65. Voordouw, G., Armstrong, S. M., Reimer, M. F., Fouts, B., Telang, A. J., Shen, Y., et al. (1996). Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulfate-reducing, fermentative, and sulfide-oxidizing bacteria. Appl. Environ. Microbiol. 62, 1623-1629
66. Wang, L.-Y., Ke, W-J., Sun, X.-B., Liu, J.-F., Gu, J.-D., and Mu, B.-Z. (2014). Comparison of bacterial community in aqueous and oil phases of water-flooded petroleum reservoirs using pyrosequencing and clone library approaches. Appl. Microbiol. Biotechnol. 98, 4209-4221. doi: 10.1007/s00253-013-5472-y
67. Weisburg, W. G., Barns, S. M., Pelletier, D. A., and Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173, 697-703. doi: 10.1128/jb.173.2.697-703.1991
68. Yamada, T., Imachi, H., Ohashi, A., Harada, H., Hanada, S., Kamagata, Y., et al. (2007). Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia. Int. J. Syst. Evol. Microbiol. 57, 2299-2306. doi: 10.1099/ijs.0.65098-0
69. Yang, Y., Wang, J., Liao, J., Xie, S., and Huang, Y. (2015). Abundance and diversity of soil petroleum hydrocarbon-degrading microbial communities in oil exploring areas. Appl. Microbiol. Biotechnol. 99, 1935-1946. doi: 10.1007/s00253-014-6074-z
70. Youssef, N., Elshahed, M. S., and McInerney, M. J. (2009a). "Microbial processes in oil fields: culprits, problems and opportunities," in: Advances in Applied Microbiology, Vol. 66, eds A. I. Laskin, S. Sariaslani, and G. M. Gadd (Burlington: Academic Press), 141-251
71. Youssef, N., Sheik, C. S., Krumholz, L. R., Najar, F. Z., Roe, B. A., and Elshahed, M. S. (2009b). Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl. Environ. Microbiol. 75, 5227-5236. doi: 10.1128/AEM.00592-09