Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front Envir Sci Eng    2013, Vol. 7 Issue (4) : 559-567
Response of bacterial communities to short-term pyrene exposure in red soil
Jingjing PENG1, Hong LI2, Jianqiang SU1, Qiufang ZHANG1, Junpeng RUI3, Chao CAI1()
1. Key Laboratory of Urban Environment and Health Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China; 2. Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK; 3. College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
 Download: PDF(331 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Pyrene, a representative polycyclic aromatic hydrocarbon (PAH) compound produced mainly from incomplete combustion of fossil fuels, is hazardous to ecosystem health. However, long-term exposure studies did not detect any significant effects of pyrene on soil microorganism. In this study, short-term microcosm experiments were conducted to identify the immediate effect of pyrene on soil bacterial communities. A freshly-collected pristine red soil was spiked with pyrene at 0, 10, 100, 200, and 500 mg·kg-1 and incubated for one day and seven days. The bacterial communities in the incubated soils were analyzed using 16S rRNA sequencing and terminal restriction fragment length polymorphism (T-RFLP) methods. The results revealed high bacterial diversity in both unspiked and pyrene-spiked soils. Only at the highest pyrene-spiking rate of 500 mg·kg-1, two minor bacteria groups of the identified 14 most abundant bacteria groups were completely suppressed. Short-term exposure to pyrene resulted in dominance of Proteobacteria in soil, followed by Acidobacteria, Firmutes, and Bacteroidetes. Our findings showed that bacterial community structure did respond to the presence of pyrene but recovered rapidly from the perturbation. The intensity of impact and the rate of recovery showed some pyrene dosage-dependent trends. Our results revealed that different levels of pyrene may affect the bacterial community structure by suppressing or selecting certain groups of bacteria. It was also found that the bacterial community was most susceptible to pyrene within one day of the chemical addition.

Keywords pyrene      bacterial communities      terminal restriction fragment length polymorphism      short-term exposure      rank-abundance plots     
Corresponding Authors: CAI Chao,   
Issue Date: 01 August 2013
 Cite this article:   
Jingjing PENG,Hong LI,Jianqiang SU, et al. Response of bacterial communities to short-term pyrene exposure in red soil[J]. Front Envir Sci Eng, 2013, 7(4): 559-567.
Fig.1  Pyrene concentration in treatments after incubation for 1 d (white) and 7 d (black). Lower-case letters indicate the outcome of an one way-ANOVA analysis comparing 1 d and 7 d values. Data are means±standard deviation of triplicate measurements
phylogenetic groupcontrol500 mg·kg-1 pyrenerelative abundance of control /(% of total taxa)relative abundance with 500 mg·kg-1 pyrene /(% of total taxa)
unclassified bacteria332.02.6
total (all taxa)147116100.0100.0
Tab.1  Phylogenetic assignments of 16S rRNA gene clones on day 1st
Fig.2  Structure of the bacterial community in red soil on day 1st (a) and day 7th (b) after addition of different doses of pyrene. The graphs show the relative abundances of T-RFs used as a measure of the composition of the bacterial community. Data are means±standard deviation of triplicate measurements
Fig.3  Phylogenetic relationship between representative bacterial 16S rRNA gene clone sequences generated from unspiked (control) and 500 mg·kg pyrene-spiked soils. Bootstrap values (for 1000 reactions) over 50% are indicated on branches. Genbank accession numbers of sequences are indicated; the in silico T-RFs size is given in square brackets
Fig.4  Changes in community structure in different treatments (0, 10, 100, 200, and 500 mg·kg) visualized using rank-abundance plots after different incubation time (day 1st (a) and day 7th (b)). Triplicate plots, the mean slope values and the standard deviation of the mean ( = 3) for each treatment are shown. All regression coefficients were significant (<0.05)
pyrene concentrationday1st/day7thday1st control/ day1st treatmentsday7th control/day7th treatments
0 ppm0.2220.150
10 ppm0.0740.2500.2900.1500.1900.150
100 ppm0.1850.3500.2000.001a)0.8500.001a)
200 ppm0.6290.001a)0.5600.001a)0.7000.001a)
500 ppm0.5560.001a)0.4100.001a)0.4800.001a)
Tab.2  β diversity index analysis. Given are the ANOSIM test statistic () and significance ()
1 Head I M, Jones D M, R?ling W F M. Marine microorganisms make a meal of oil. Nature Reviews Microbiology , 2006, 4(3): 173–182
doi: 10.1038/nrmicro1348 pmid:16489346
2 Su Y H, Zhu Y G. Uptake of selected PAHs from contaminated soils by rice seedlings (Oryza sativa) and influence of rhizosphere on PAH distribution. Environmental Pollution , 2008, 155(2): 359–365
doi: 10.1016/j.envpol.2007.11.008 pmid:18331768
3 Tao Y Q, Zhang S Z, Zhu Y G, Christie P. Uptake and acropetal translocation of polycyclic aromatic hydrocarbons by wheat (Triticum aestivum L.) grown in field-contaminated soil. Environmental Science &amp; Technology , 2009, 43(10): 3556–3560
doi: 10.1021/es803368y pmid:19544854
4 Cerniglia C E. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation , 1992, 3(2-3): 351–368
doi: 10.1007/BF00129093
5 Vi?as M, Sabaté J, Espuny M J, Solanas A M. Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Applied and Environmental Microbiology , 2005, 71(11): 7008–7018
doi: 10.1128/AEM.71.11.7008-7018.2005 pmid:16269736
6 Ben Said O, Go?i-Urriza M, El Bour M, Aissa P, Duran R. Bacterial community structure of sediments of the bizerte lagoon (Tunisia), a southern Mediterranean coastal anthropized lagoon. Microbial Ecology , 2010, 59(3): 445–456
doi: 10.1007/s00248-009-9585-x pmid:19789910
7 Deng H, Li X F, Cheng W D, Zhu Y G. Resistance and resilience of Cu-polluted soil after Cu perturbation, tested by a wide range of soil microbial parameters. FEMS Microbiology Ecology , 2009, 70(2): 137–148
doi: 10.1111/j.1574-6941.2009.00741.x pmid:19663920
8 Paissé S, Coulon F, Go?i-Urriza M, Peperzak L, McGenity T J, Duran R. Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment. FEMS Microbiology Ecology , 2008, 66(2): 295–305
doi: 10.1111/j.1574-6941.2008.00589.x pmid:18803671
9 Yang H, Su Y H, Zhu Y G, Chen M M, Chen B D, Liu Y X. Influences of polycyclic aromatic hydrocarbons (PAHs) on soil microbial community composition with or without Vegetation. Journal of Environmental Science and Health Part A-Toxic/Hazardous Substances &amp; Environmental Engineering , 2007, 42(1): 65–72
10 Gao Y Z, Ling W T, Wong M H. Plant-accelerated dissipation of phenanthrene and pyrene from water in the presence of a nonionic-surfactant. Chemosphere , 2006, 63(9): 1560–1567
doi: 10.1016/j.chemosphere.2005.09.058 pmid:16581106
11 Lin Y T, Huang Y J, Tang S L, Whitman W B, Coleman D C, Chiu C Y. Bacterial community diversity in undisturbed perhumid montane forest soils in Taiwan. Microbial Ecology , 2010, 59(2): 369–378
doi: 10.1007/s00248-009-9574-0 pmid:19727930
12 Zhang W, Wang H, Zhang R, Yu X Z, Qian P Y, Wong M H. Bacterial communities in PAH contaminated soils at an electronic-waste processing center in China. Ecotoxicology (London, England) , 2010, 19(1): 96–104
doi: 10.1007/s10646-009-0393-3 pmid:19633954
13 Sverdrup L E, Ekelund F, Krogh P H, Nielsen T, Johnsen K. Soil microbial toxicity of eight polycyclic aromatic compounds: effects on nitrification, the genetic diversity of bacteria, and the total number of protozoans. Environmental Toxicology and Chemistry , 2002, 21(8): 1644–1650
doi: 10.1002/etc.5620210815 pmid:12152764
14 Peng J J, Cai C, Qiao M, Li H, Zhu Y G. Dynamic changes in functional gene copy numbers and microbial communities during degradation of pyrene in soils. Environmental Pollution , 2010, 158(9): 2872–2879
doi: 10.1016/j.envpol.2010.06.020 pmid:20615597
15 Ager D, Evans S, Li H, Lilley A K, van der Gast C J. Anthropogenic disturbance affects the structure of bacterial communities. Environmental Microbiology , 2010, 12(3): 670–678
doi: 10.1111/j.1462-2920.2009.02107.x pmid:20002134
16 Maliszewska-Kordybach B, Klimkowicz-Pawlas A, Smreczak B, Janusauskaite D. Ecotoxic effect of phenanthrene on nitrifying bacteria in soils of different properties. Journal of Environmental Quality , 2007, 36(6): 1635–1645
doi: 10.2134/jeq2007.0118 pmid:17940263
17 Weisburg W G, Barns S M, Pelletier D A, Lane D J. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology , 1991, 173(2): 697–703
18 Rui J P, Peng J J, Lu Y H. Succession of bacterial populations during plant residue decomposition in rice field soil. Applied and Environmental Microbiology , 2009, 75(14): 4879–4886
doi: 10.1128/AEM.00702-09 pmid:19465536
19 Osborne C A, Rees G N, Bernstein Y, Janssen P H. New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Applied and Environmental Microbiology , 2006, 72(2): 1270–1278
doi: 10.1128/AEM.72.2.1270-1278.2006 pmid:16461676
20 Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution , 2007, 24(8): 1596–1599
doi: 10.1093/molbev/msm092 pmid:17488738
21 Lilley A K, Fry J C, Bailey M J, Day M J. Comparison of aerobic heterotrophic taxa isolated from four root domains of mature sugar beet (Beta vulgaris). FEMS Microbiology Ecology , 1996, 21(3): 231–242
doi: 10.1111/j.1574-6941.1996.tb00350.x
23 van der Gast C J, Walker A W, Stressmann F A, Rogers G B, Scott P, Daniels T W, Carroll M P, Parkhill J, Bruce K D. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. The ISME Journal, 2011, 5(5): 780–791
doi: 10.1038/ismej.2010.175 pmid:21151003
24 Bell T, Ager D, Song J I, Newman J A, Thompson I P, Lilley A K, van der Gast C J. Larger islands house more bacterial taxa. Science , 2005, 308(5730): 1884
doi: 10.1126/science.1111318 pmid:15976296
25 Clarke K R. Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology , 1993, 18(1): 117–143
doi: 10.1111/j.1442-9993.1993.tb00438.x
26 Nakatsu C H, Torsvik V, Ovreas L. Soil community analysis using DGGE of 16S rDNA polymerase chain reaction products. Soil Science Society of America Journal , 2000, 64(4): 1382–1388
doi: 10.2136/sssaj2000.6441382x
27 Wang X J, Yang J, Chen X P, Sun G X, Zhu Y G. Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. Journal of Soils and Sediments , 2009, 9(6): 568–577
doi: 10.1007/s11368-009-0113-x
28 Singleton D R, Richardson S D, Aitken M D. Effects of enrichment with phthalate on polycyclic aromatic hydrocarbon biodegradation in contaminated soil. Biodegradation , 2008, 19(4): 577–587
doi: 10.1007/s10532-007-9163-1 pmid:17990065
29 Singleton D R, Sangaiah R, Gold A, Ball L M, Aitken M D. Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environmental Microbiology , 2006, 8(10): 1736–1745
doi: 10.1111/j.1462-2920.2006.01112.x pmid:16958754
30 Yrj?l? K, Keskinen A K, Akerman M L, Fortelius C, Sipil? T P. The rhizosphere and PAH amendment mediate impacts on functional and structural bacterial diversity in sandy peat soil. Environmental Pollution , 2010, 158(5): 1680–1688
doi: 10.1016/j.envpol.2009.11.026 pmid:20022155
31 Macleod C J A, Semple K T. The adaptation of two similar soils to pyrene catabolism. Environmental Pollution , 2002, 119(3): 357–364
doi: 10.1016/S0269-7491(01)00343-8 pmid:12166669
32 Hartmann M, Widmer F. Community structure analyses are more sensitive to differences in soil bacterial communities than anonymous diversity indices. Applied and Environmental Microbiology , 2006, 72(12): 7804–7812
doi: 10.1128/AEM.01464-06 pmid:17041161
33 Girvan M S, Campbell C D, Killham K, Prosser J I, Glover L A. Bacterial diversity promotes community stability and functional resilience after perturbation. Environmental Microbiology , 2005, 7(3): 301–313
doi: 10.1111/j.1462-2920.2005.00695.x pmid:15683391
[1] Wendi XU,Shuhai GUO,Gang LI,Fengmei LI,Bo WU,Xinhong GAN. Combination of the direct electro-Fenton process and bioremediation for the treatment of pyrene-contaminated soil in a slurry reactor[J]. Front. Environ. Sci. Eng., 2015, 9(6): 1096-1107.
[2] Xunan YANG, Shan HUANG, Qunhe WU, Renduo ZHANG, Guangli LIU. Diversity and vertical distributions of sediment bacteria in an urban river contaminated by nutrients and heavy metals[J]. Front Envir Sci Eng, 2013, 7(6): 851-859.
[3] Shuang LIU, Yanwei HOU, Guoxin SUN. Synergistic degradation of pyrene and volatilization of arsenic by cocultures of bacteria and a fungus[J]. Front Envir Sci Eng, 2013, 7(2): 191-199.
[4] Dawen GAO, Yu TAO. Current molecular biologic techniques for characterizing environmental microbial community[J]. Front Envir Sci Eng, 2012, 6(1): 82-97.
[5] Xiaohui WANG, Xianghua WEN, Hengjing YAN, Kun DING, Man HU. Community dynamics of ammonia oxidizing bacteria in a full-scale wastewater treatment system with nitrification stability[J]. Front Envir Sci Eng Chin, 2011, 5(1): 92-98.
[6] Hongyuan WANG, Xiaolu JIANG, Ya HE, Huashi GUAN. Spatial and seasonal variations in bacterial communities of the Yellow Sea by T-RFLP analysis[J]. Front Envir Sci Eng Chin, 2009, 3(2): 194-199.
[7] Jin GUO, Jun MA. Pyrene partition behavior to the NOM: Effect of NOM characteristics and its modification by ozone preoxidation[J]. Front Envir Sci Eng Chin, 2009, 3(1): 56-61.
[8] SU Yuhong, YANG Xueyun, CHIOU Cary. Effect of rhizosphere on soil microbial community and pyrene biodegradation[J]. Front.Environ.Sci.Eng., 2008, 2(4): 468-474.
[9] XIA Xinghui, HU Lijuan, MENG Lihong. Adsorption and partition of benzo(a)pyrene on sediments with different particle sizes from the Yellow River[J]. Front.Environ.Sci.Eng., 2007, 1(2): 172-178.
Full text