Long-term oil contamination alters the molecular ecological networks of soil microbial functional genes

Frontiers in Microbiology

Volumn 7, Issue FEB, 2016, Pages

  Liang, Yuting ^a   Zhao, Huihui ^a   Deng, Ye ^b,c   Zhou, Jizhong ^c,d   Li, Guanghe ^b,c   Sun, Bo ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b TSINGHUA UNIVERSITY   (China)

^c RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^d UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Functional genes; Hydrocarbon degradation; Microbial interaction; Molecular ecological network; Oil contamination

Indexed keywords

ALIPHATIC HYDROCARBON; AROMATIC HYDROCARBON; NITROGEN; PHOSPHORUS;

ALKB GENE; AORL GENE; ARTICLE; BACTERIAL GENE; BPHA GENE; BPHC GENE; GENE IDENTIFICATION; GENE INTERACTION; MICROARRAY ANALYSIS; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MOLECULAR ECOLOGY; NAHA GENE; NIDA GENE; NONHUMAN; OXOH GENE; PH; PHDJ GENE; SOIL MICROFLORA; SOIL POLLUTION; TOTAL ORGANIC CARBON; WATER CONTENT;

EID: 84962086570     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00060     Document Type: Article

References (72)

1. Albert, R., Jeong, H., and Barabasi, A. L. (2000). Error and attack tolerance of complex networks. Nature 406, 378-382. doi: 10.1038/35019019
2. Atlas, R. (1981). Microbial-degradation of petroleumhydrocarbons: an environmental perspective. Microbiol. Rev. 45, 180-209.
3. Baldwin, B. R., Nakatsu, C. H., and Nies, L. (2008). Enumeration of aromatic oxygenase genes to evaluate monitored natural attenuation at gasoline-contaminated site. Water Res. 42, 723-731. doi: 10.1016/j.watres.2007.07.052
4. Barberan, A., Bates, S. T., Casamayor, E. O., and Fierer, N. (2012). Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 6, 343-351. doi: 10.1038/ismej.2011.119
5. Bell, T. H., Callender, K. L., Whyte, L. G., and Greer, C. W. (2013a). Microbial competition in polar soils: a review of an understudied but potentially important control on productivity. Biology 2, 533-554. doi: 10.3390/biology2020533
6. Bell, T. H., Yergeau, E., Maynard, C., Juck, D., Whyte, L. G., and Greer, C. W. (2013b). Predictable bacterial composition and hydrocarbon degradation in Arctic soils following diesel and nutrient disturbance. ISME J. 7, 1200-1210. doi: 10.1038/ismej.2013.1
7. Bell, T. H., Hassan, S. E., Lauron-Moreau, A. L., Al-Otaibi, F., Hijri, M., Yergeau, E., et al. (2014). Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME J. 8, 331-343. doi: 10.1038/ismej.2013.149
8. Bell, T. H., Yergeau, E., Martineau, C., Juck, D., Whyte, L. G., and Greer, C. W. (2011). Identification of nitrogen-incorporating bacteria in petroleum-contaminated arctic soils by using [15N]DNA-based stable isotope probing and pyrosequencing. Appl. Environ. Microbiol. 77, 4163-4171. doi: 10.1128/AEM.00172-11
9. Cavalca, L., Dell Amico, E., and Andreoni, V. (2004). Intrinsic bioremediability of an aromatic hydrocarbon-polluted groundwater: diversity of bacterial populations and toluene monoxygenase genes. Appl. Microbiol. Biotechnol. 64, 576-587. doi: 10.1007/s00253-003-1449-6
10. Cébron, A., Norini, M. P., Beguiristain, T., and Leyval, C. (2008). Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDa) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J. Microbiol. Methods 73, 148-159. doi: 10.1016/j.mimet.2008.01.009
11. Chaillana, F., Le Flècheb, A., Burya, E., Phantavonga, Y., Grimontb, P., Saliotc, A., et al. (2004). Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res. Microbiol. 155, 587-595. doi: 10.1016/j.resmic.2004.04.006
12. Clauset, A., Newman, M., and Moore, C. (2004). Finding community structure in very large networks. Phys. Rev. E 70, 066111. doi: 10.1103/PhysRevE.70.066111
13. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., et al. (2007). Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366-2382. doi: 10.1038/nprot.2007.324
14. Das, N., and Chandran, P. (2011). Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol. Res. Int. 2011, 1-13. doi: 10.4061/2011/941810
15. Dionisi, H. M., Chewning, C. S., Morgan, K. H., Menn, F. M., Easter, J. P., and Sayler, G. S. (2004). Abundance of dioxygenase genes similar to Ralstonia sp. strain U2 nagAc is correlated with naphthalene concentrations in coal tar-contaminated freshwater sediments. Appl. Environ. Microbiol. 70, 3988-3995. doi: 10.1128/AEM.70.7.3988-3995.2004
16. Faust, K., and Raes, J. (2012). Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538-550. doi: 10.1038/nrmicro2832
17. Fleming, J. T., John Sanseverino, S., and Sayler, G. S. (1993). Quantitative relationship between naphthalene catabolic gene frequency and expression in predicting PAH degradation in soils at town gas manufacturing sites. Environ. Sci. Technol. 41, 1068-1074. doi: 10.1021/es00043a005
18. Fuhrman, J. A., and Steele, J. A. (2008). Community structure of marine bacterioplankton: patterns, networks, and relationships to function. Aquat. Microb. Ecol. 53, 69-81. doi: 10.3354/ame01222
19. Garland, J. L., and Mills, A. L. (1991). Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl. Environ. Microbiol. 57, 2351-2359.
20. Guimera, R., and Amaral, L. (2005). Functional cartography of complex metabolic networks. Nature 433, 895-900. doi: 10.1038/nature03288
21. Guimera, R., Sales-Pardo, M., and Amaral, L. A. N. (2007). Classes of complex networks defined by role-to-role connectivity profiles. Nat. Phys. 3, 63-69. doi: 10.1038/nphys489
22. Hamamura, N., Ward, D., and Inskeep, W. (2013). Effects of petroleum mixture types on soil bacterial population dynamics associated with the biodegradation of hydrocarbons in soil environments. FEMS Microbiol. Ecol. 85, 168-178. doi: 10.1111/1574-6941.12108
23. Hartwell, L. H., Hopfield, J. J., Leibler, S., and Murray, A. W. (1999). From molecular to modular cell biology. Nature 402(6761 Suppl), C47-C52. doi: 10.1038/35011540
24. Hazen, T. C., Dubinsky, E. A., Desantis, T. Z., Andersen, G. L., Piceno, Y. M., Singh, N., et al. (2010). Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204-208. doi: 10.1126/science.1195979
25. He, Z., Van Nostrand, J. D., and Zhou, J. (2012). Applications of functional gene microarrays for profiling microbial communities. Curr. Opin. Biotechnol. 23, 460-466. doi: 10.1016/j.copbio.2011.12.021
26. He, Z. L., Deng, Y., Van Nostrand, J. D., Tu, Q. C., Xu, M. Y., Hemme, C. L., et al. (2010). GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. ISME J. 4, 1167-1179. doi: 10.1038/ismej.2010.46
27. Horvath, R. S. (1972). Microbial co-metabolism and the degradation of organic compounds in nature. Bacteriol. Rev. 36, 146-155.
28. Horvath, S., and Dong, J. (2008). Geometric interpretation of gene coexpression network analysis. PLoS Comput. Biol. 4:e1000117. doi: 10.1371/journal.pcbi.1000117
29. Horvath, S., Zhang, B., Carlson, M., Lu, K. V., Zhu, S., Felciano, R. M., et al. (2006). Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc. Natl. Acad. Sci. U.S.A. 103, 17402-17407. doi: 10.1073/pnas.0608396103
30. Kingston, P. F. (2002). Long-term environmental impact of oil spills. Spill Sci. Technol. Bull. 7, 53-61. doi: 10.1016/S1353-2561(02)00051-8
31. Kvenvolden, K. A., and Cooper, C. K. (2003). Natural seepage of crude oil into the marine environment. Geo-Mar. Lett. 23, 140-146. doi: 10.1007/s00367-003-0135-0
32. Labud, V., Garcia, C., and Hernandez, T. (2007). Effect of hydrocarbon pollution on the microbial properties of a sandy and a clay soil. Chemosphere 66, 1863-1871. doi: 10.1016/j.chemosphere.2006.08.021
33. Liang, Y., Van Nostrand, J. D., Deng, Y., He, Z., Wu, L., Zhang, X., et al. (2011). Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J. 5, 403-413. doi: 10.1038/ismej.2010.142
34. Liang, Y., Zhang, X., Wang, J., and Li, G. (2012). Spatial variations of hydrocarbon contamination and soil properties in oil exploring fields across China. J. Hazard. Mater. 241, 371-378. doi: 10.1016/j.jhazmat.2012.09.055
35. Liang, Y. T., Zhang, X., Zhou, J., and Li, G. (2010). Long-term oil contamination increases deterministic assembly processes in soil microbes. Appl. Environ. Microbiol. 76, 1088-1094. doi: 10.1128/AEM.02749-09
36. Liang, Y., Zhang, X., Zhou, J., and Li, G. (2015). Long-term oil contamination increases deterministic assembly processes in soil microbes. Ecol. Appl. 25, 1235-1243. doi: 10.1890/14-1672.1
37. Lu, Z., Deng, Y., Van Nostrand, J. D., He, Z., Voordeckers, J., Tom, M. L., et al. (2012). Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume. ISME J. 6, 451-460. doi: 10.1038/ismej.2011.91
38. Luo, F., Yang, Y., Zhong, J., Gao, H., Khan, L., Thompson, D. K., et al. (2007). Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory. BMC Bioinformatics 8:299. doi: 10.1186/1471-2105-8-299
39. Luo, F., Zhong, J., Yang, Y., Scheuermann, R. H., and Zhou, J. (2006). Application of random matrix theory to biological networks. Phys. Lett. A 357, 420-423. doi: 10.1016/j.physleta.2006.04.076
40. Marlowe, E. M., Wang, J. M., Pepper, I. L., and Maier, R. M. (2002). Application of reverse transcription-PCR assay to monitor regulation of the catabolic nahAc gene during phenanthrene degradation. Biodegradation 13, 251-260. doi: 10.1023/A:1021221104425
41. Maslov, S., and Sneppen, K. (2002). Specificity and stability in topology of protein networks. Science 296, 910-913. doi: 10.1126/science.1065103
42. Mason, O. U., Hazen, T. C., Borglin, S., Chain, P. S., Dubinsky, E. A., Fortney, J. L., et al. (2012). Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J. 6, 1715-1727. doi: 10.1038/ismej.2012.59
43. Meidute, S., Demoling, F., and Baath, E. (2008). Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biol. Biochem. 40, 2334-2343. doi: 10.1016/j.soilbio.2008.05.011
44. Mesarch, M. B., Nakatsu, C. H., and Nies, L. (2004). Bench-scale and field-scale evaluation of catechol 2, 3-dioxygenase specific primers for monitoring BTX bioremediation. Water Res. 38, 1281-1288. doi: 10.1016/j.watres.2003.10.052
45. Meyneta, P., Moliternic, E., Davenporta, R. J., Sloanb, W. T., Camachoc, J. V., and Werner, D. (2014). Predicting the effects of biochar on volatile petroleum hydrocarbon biodegradation and emanation from soil: a bacterial community finger-print analysis inferred modelling approach. Soil Biol. Biochem. 68, 20-30. doi: 10.1016/j.soilbio.2013.09.015
46. Mille-Lindblom, C., Fischer, H., and Tranvik, L. J. (2006). Antagonism between bacteria and fungi: substrate competition and a possible tradeoffbetween fungal growth and tolerance towards bacteria. Oikos 113, 233-242. doi: 10.1111/j.2006.0030-1299.14337.x
47. Mohanty, G., and Mukherji, S. (2008). Biodegradation rate of diesel range n-alkanes by bacterial cultures Exiguobacterium aurantiacum and Burkholderia cepacia. Int. Biodeter. Biodegradation 61, 240-250. doi: 10.1016/j.ibiod.2007.06.011
48. Montoya, J. M., Pimm, S. L., and Sole, R. V. (2006). Ecological networks and their fragility. Nature 442, 259-264. doi: 10.1038/nature04927
49. Moore, D., and Dowhan, D. (2002). Purification and concentration of DNA from aqueous solutions. Curr. Protoc. Mol. Biol. Chap. 2, Unit2.1A.
50. Mougi, A., and Kondoh, M. (2012). Diversity of interaction types and ecological community stability. Science 337, 349-351. doi: 10.1126/science.1220529
51. Naïtali, M. B., Rakatozafy, H., Marchal, R., Leveau, J. Y., and Vandecasteele, J. P. (2003). Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J. Appl. Microbiol. 86, 421-428. doi: 10.1046/j.1365-2672.1999.00678.x
52. Nzila, A. (2013). Update on the cometabolism of organic pollutants by bacteria. Environ. Pollut. 178, 474-482. doi: 10.1016/j.envpol.2013.03.042
53. Park, J. W., and Crowley, D. E. (2006). Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl. Microbiol. Biot. 72, 1322-1329. doi: 10.1007/s00253-006-0423-5
54. Penton, C. R., Johnson, T. A., Quensen, J. F., Iwai, S., Cole, J. R., and Tiedje, J. M. (2013). Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: primers and processing matter. Front. Microbiol. 4:279. doi: 10.3389/fmicb.2013.00279
55. Raes, J., and Bork, P. (2008). Systems microbiology-Timeline-Molecular eco-systems biology: towards an understanding of community function. Nat. Rev. Microbiol. 6, 693-699. doi: 10.1038/nrmicro1935
56. Raes, J., Foerstner, K. U., and Bork, P. (2007). Get the most out of your metagenome: computational analysis of environmental sequence data. Curr. Opin. Microbiol. 10, 490-498. doi: 10.1016/j.mib.2007.09.001
57. Ringelberg, D. B., Talley, J. W., Perkins, E. J., Tucker, S. G., Luthy, R. G., Bouwer, E. J., et al. (2001). Succession of phenotypic, genotypic, and metabolic community characteristics during in vitro bioslurry treatment of polycyclic aromatic hydrocarbon-contaminated sediments. Appl. Environ. Microb. 67, 1542-1550. doi: 10.1128/AEM.67.4.1542-1550.2001
58. Rousk, J., Demoling, L. A., Bahr, A., and Baath, E. (2008). Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol. Ecol. 63, 350-358. doi: 10.1111/j.1574-6941.2008.00440.x
59. Salminen, J. M., Tuomi, P. M., and Jørgensen, K. S. (2008). Functional gene abundances (nahAc, alkB, xylE) in the assessment of the efficacy of bioremediation. Appl. Biochem. Microbiol. 151, 638-652. doi: 10.1007/s12010-008-8275-3
60. Sei, K., Sugimoto, Y., Mori, K., Maki, H., and Kohno, T. (2003). Monitoring of alkane degrading bacteria in a sea-water microcosm during crude oil degradation by polymerase chain reaction based on alkane-catabolic genes. Environ. Microbiol. 5, 517-522. doi: 10.1046/j.1462-2920.2003.00447.x
61. Simon, C., and Daniel, R. (2011). Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77, 1153-1161. doi: 10.1128/AEM.02345-10
62. Stapleton, R. D., and Sayler, G. S. (2000). Changes in subsurface catabolic gene frequences during natural attenuation of petroleum hydrocarbons. Environ. Sci. Technol. 69, 461-467.
63. Steele, J. A., Countway, P. D., Xia, L., Vigil, P. D., Beman, J. M., Kim, D. Y., et al. (2011). Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J. 5, 1414-1425. doi: 10.1038/ismej.2011.24
64. Tu, Q., Yu, H., He, Z., Deng, Y., Wu, L., Van Nostrand, J. D., et al. (2014). GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol. Ecol. Resour. 14, 914-928. doi: 10.1111/1755-0998.12239
65. Tuomi, M., Salminen, J. M., and Jorgensen, K. S. (2004). The abundance of nahAc genes correlates with the 14C-naphthalene mineralization potential in petroleum hydrocarbon-contaminated oxic soil layers. FEMS Microbiol. Ecol. 51, 99-107. doi: 10.1016/j.femsec.2004.07.011
66. Van Hamme, J. D., Singh, A., and Ward, O. P. (2003). Recent advances in petroleum microbiology. Microbiol. Mol. Biol. Rev. 67, 503-549. doi: 10.1128/MMBR.67.4.503-549.2003
67. Violle, C., Pu, Z., and Jiang, L. (2010). Experimental demonstration of the importance of competition under disturbance. Proc. Natl. Acad. Sci. U.S.A. 107, 12925-12929. doi: 10.1073/pnas.1000699107
68. West, D. B. (1996). Introduction to Graph Theory. Upper Saddle River, NJ: Prentice Hall Inc.
69. Yergeau, E., Kang, S., He, Z., Zhou, J., and Kowalchuk, G. A. (2007). Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J. 1, 163-179. doi: 10.1038/ismej.2007.24
70. Zhou, J. Z., Bruns, M. A., and Tiedje, J. M. (1996). DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316-322.
71. Zhou, J., Deng, Y., Luo, F., He, Z., Tu, Q., and Zhi, X. (2010). Functional molecular ecological networks. MBio 1, e169-e110. doi: 10.1128/mBio.00169-10
72. Zhou, J., He, Z., Yang, Y., Deng, Y., Tringe, S. G., and Alvarez-Cohen, L. (2015). High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio 6, e02288-14. doi: 10.1128/mBio.02288-14