Advertisement

Biology and Fertility of Soils

, Volume 54, Issue 5, pp 607–616 | Cite as

Niche partition of phenanthrene-degrading bacteria along a Phragmites australis rhizosphere gradient

  • Xiaofei Lv
  • Zhao Kankan
  • Hongjie Li
  • Bin Ma
Original Paper

Abstract

The rhizosphere is a critical interface for pollutant remediation in soils. Association between biodegradation of organic pollutants and spatial pattern of degraders along the rhizosphere gradient is, however, still unclear. This study investigated the phenanthrene-degrading bacterial consortia in a Phragmites australis rhizosphere using DNA-stable isotope probing (DNA-SIP). The relative abundance of Sphingomonadales in the 13C-labeled consortia decreased with the distance from roots, suggesting that its contribution in phenanthrene degradation was decreased with the distance from roots. Conversely, the relative abundance of Rhizobiales, Rhodobacterales, Lactobacillales, and Enterobacteriales in 13C-labeled consortia increased with the distance from roots, suggesting that their contributions in phenanthrene degradation were increased with the distance from roots. The linkage numbers of bacterial species in the co-occurrence network increased with the percentages of 13C-labeled reads, suggesting the critical role of syntrophic interactions for phenanthrene degraders. These results suggest the niche partition of phenanthrene degraders, which leaded to the non-linear variation of phenanthrene degradation rates along the rhizosphere gradient. These findings will help us to better understand rhizo degradation of organic pollutants and optimize bioremediation technology by achieving a trade-off among different degraders.

Keywords

Bioremediation Correlation network Phenanthrene Rhizosphere gradient Stable isotope probing 

Notes

Funding information

This work was supported by the National Natural Science Foundation of China (41301333), the China Postdoctoral Science Foundation (2017 M621945), and the Fundamental Research Funds for the Central Universities (2018QNA6009).

References

  1. Cébron A, Louvel B, Faure P, France-Lanord C, Chen Y, Murrell JC, Leyval C (2011) Root exudates modify bacterial diversity of phenanthrene degraders in PAH-polluted soil but not phenanthrene degradation rates. Environ Microbiol 13:722–736CrossRefPubMedGoogle Scholar
  2. Chakraborty R, Borglin SE, Dubinsky EA, Andersen GL, Hazen TC (2012) Microbial response to the MC-252 oil and Corexit 9500 in the Gulf of Mexico. Front Microbiol 3:357PubMedPubMedCentralGoogle Scholar
  3. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefPubMedGoogle Scholar
  4. El Amrani A, Dumas A-S, Wick LY, Yergeau E, Berthomé R (2015) “Omics” insights into PAH degradation toward improved green remediation biotechnologies. Environ Sci Technol 49:11281–11291CrossRefPubMedGoogle Scholar
  5. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550.  https://doi.org/10.1038/nrmicro2832 CrossRefPubMedGoogle Scholar
  6. Feizi S, Marbach D, Médard M, Kellis M (2013) Network deconvolution as a general method to distinguish direct dependencies in networks. Nat Biotechnol 31:726–733CrossRefPubMedPubMedCentralGoogle Scholar
  7. Gao Y, Ren L, Ling W, Gong S, Sun B, Zhang Y (2010) Desorption of phenanthrene and pyrene in soils by root exudates. Bioresour Technol 101:1159–1165CrossRefPubMedGoogle Scholar
  8. Gerhardt KE, Huang X-D, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30CrossRefGoogle Scholar
  9. Gieg LM, Fowler SJ, Berdugo-Clavijo C (2014) Syntrophic biodegradation of hydrocarbon contaminants. Curr Opin Biotechnol 27:21–29.  https://doi.org/10.1016/j.copbio.2013.09.002 CrossRefPubMedGoogle Scholar
  10. He Y, Xu J, Tang C, Wu Y (2005) Facilitation of pentachlorophenol degradation in the rhizosphere of ryegrass (Lolium perenne l.). Soil Biol Biochem 37:2017–2024CrossRefGoogle Scholar
  11. He Y, Xu J, Ma Z, Wang H, Wu Y (2007) Profiling of PLFA: implications for nonlinear spatial gradient of PCP degradation in the vicinity of Lolium perenne L. roots. Soil Biol Biochem 39:1121–1129CrossRefGoogle Scholar
  12. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84.  https://doi.org/10.1016/j.envpol.2004.04.015 CrossRefPubMedGoogle Scholar
  13. Johnson CR, Scow KM (1999) Effect of nitrogen and phosphorus addition on phenanthrene biodegradation in four soils. Biodegradation 10:43–50.  https://doi.org/10.1023/A:1008359606545 CrossRefPubMedGoogle Scholar
  14. Jones MD, Crandell DW, Singleton DR, Aitken MD (2011) Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ Microbiol 13:2623–2632CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kleinsteuber S, Schleinitz KM, Vogt C (2012) Key players and team play: anaerobic microbial communities in hydrocarbon-contaminated aquifers. Appl Microbiol Biotechnol 94:851–873CrossRefPubMedGoogle Scholar
  16. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schäberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K (2015) A new antibiotic kills pathogens without detectable resistance. Nature 517:455–459.  https://doi.org/10.1038/nature14098 CrossRefPubMedGoogle Scholar
  17. Ma Y, Wang L, Shao Z (2006) Pseudomonas, the dominant polycyclic aromatic hydrocarbon-degrading bacteria isolated from Antarctic soils and the role of large plasmids in horizontal gene transfer. Environ Microbiol 8:455–465CrossRefPubMedGoogle Scholar
  18. Ma B, He Y, Chen H, Xu J, Rengel Z (2010) Dissipation of polycyclic aromatic hydrocarbons (PAHs) in the rhizosphere: synthesis through meta-analysis. Environ Pollut 158:855–861CrossRefPubMedGoogle Scholar
  19. Ma B, Wang J, Xu M, He Y, Wang H, Wu L, Xu J (2012) Evaluation of dissipation gradients of polycyclic aromatic hydrocarbons in rice rhizosphere utilizing a sequential extraction procedure. Environ Pollut 162:413–421CrossRefPubMedGoogle Scholar
  20. Ma B, Lyu XF, Zha T, Gong J, He Y, Xu JM (2015) Reconstructed metagenomes reveal changes of microbial functional profiling during PAHs degradation along a rice (Oryza sativa) rhizosphere gradient. J Appl Microbiol 118:890–900CrossRefPubMedGoogle Scholar
  21. Magee BR, Lion LW, Lemley AT (1991) Transport of dissolved organic macromolecules and their effect on the transport of phenanthrene in porous media. Environ Sci Technol 25:323–331CrossRefGoogle Scholar
  22. Martin F, Torelli S, Le Paslier D, Barbance A, Martin-Laurent F, Bru D, Geremia R, Blake G, Jouanneau Y (2012) Betaproteobacteria dominance and diversity shifts in the bacterial community of a PAH-contaminated soil exposed to phenanthrene. Environ Pollut 162:345–353CrossRefPubMedGoogle Scholar
  23. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531.  https://doi.org/10.1371/journal.pcbi.1003531 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Peng R-H, Xiong A-S, Xue Y, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955.  https://doi.org/10.1111/j.1574-6976.2008.00127.x CrossRefPubMedGoogle Scholar
  25. Perisin M, Vetter M, Gilbert JA, Bergelson J (2015) 16Stimator: statistical estimation of ribosomal gene copy numbers from draft genome assemblies. ISME J 10:1020–1024CrossRefPubMedPubMedCentralGoogle Scholar
  26. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799.  https://doi.org/10.1038/nrmicro3109 CrossRefPubMedGoogle Scholar
  27. Regonne RK, Martin F, Mbawala A, Ngassoum MB, Jouanneau Y (2013) Identification of soil bacteria able to degrade phenanthrene bound to a hydrophobic sorbent in situ. Environ Pollut 180:145–151CrossRefPubMedGoogle Scholar
  28. Ren G, Teng Y, Ren W, Dai S, Li Z (2016) Pyrene dissipation potential varies with soil type and associated bacterial community changes. Soil Biol Biochem 103:71–85CrossRefGoogle Scholar
  29. Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fert Soil 53:485–489CrossRefGoogle Scholar
  30. Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD (2011) Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot 107:89–99.  https://doi.org/10.1093/aob/mcq221 CrossRefPubMedGoogle Scholar
  31. Singleton DR, Powell SN, Sangaiah R, Gald A, Ball LM, Aitken MD (2005) Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene, or phenanthrene in a bioreactor treating contaminated soil. Appl Environ Microbiol 71:1202–1209CrossRefPubMedPubMedCentralGoogle Scholar
  32. Song M, Jiang L, Zhang D, Luo C, Wang Y, Yu Z, Yin H, Zhang G (2016) Bacteria capable of degrading anthracene, phenanthrene, and fluoranthene as revealed by DNA based stable-isotope probing in a forest soil. J Hazard Mater 308:50–57.  https://doi.org/10.1016/j.jhazmat.2016.01.009 CrossRefPubMedGoogle Scholar
  33. Tauler M, Vila J, Nieto JM, Grifoll M (2016) Key high molecular weight PAH-degrading bacteria in a soil consortium enriched using a sand-in-liquid microcosm system. Appl Microbiol Biotechnol 100:3321–3336CrossRefPubMedGoogle Scholar
  34. Thomas F, Cébron A (2016) Short-term rhizosphere effect on available carbon sources, phenanthrene degradation, and active microbiome in an aged-contaminated industrial soil. Front Microbiol 7:92PubMedPubMedCentralGoogle Scholar
  35. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fert Soil 53:479–484CrossRefGoogle Scholar
  36. Wilcke W (2007) Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma 141:157–166CrossRefGoogle Scholar
  37. Xu M, He Z, Zhang Q, Liu J, Guo J, Sun G, Zhou J (2015) Responses of aromatic-degrading microbial communities to elevated nitrate in sediments. Environ Sci Technol 49:12422–12431.  https://doi.org/10.1021/acs.est.5b03442 CrossRefPubMedGoogle Scholar
  38. Zhang SY, Wang QF, Xie SG (2012) Molecular characterization of phenanthrene-degrading methanogenic communities in leachate-contaminated aquifer sediment. Int J Environ Sci Technol 9:705–712CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental EngineeringChina Jiliang UniversityHangzhouChina
  2. 2.Institute of Soil and Water Resources and Environmental Science, Zhejiang Provincial Key Laboratory of Agricultural Resources and EnvironmentZhejiang UniversityHangzhouChina
  3. 3.Department of BacteriologyUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations