Skip to main content
SpringerLink
Log in

Response of low-molecular-weight organic acids in mangrove root exudates to exposure of polycyclic aromatic hydrocarbons

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Low-molecular-weight organic acids (LMWOAs) represent an important component of root exudates. They play a pivotal role in the degradation of polycyclic aromatic hydrocarbons (PAHs) in sediments as they influence PAH bioavailability and degrader colonization. This study examined variations of LMWOAs in mangrove root exudates (Aegiceras corniculatum and Kandelia obovata) after exposure in phenanthrene and pyrene solution for 7 and 40 days, respectively. After 7 days of treatment, total root exudates and six types of LMWOA in root exudates from both mangrove species were enhanced. The largest increase was found in oxalic acid, i.e., the dominant component in determined LMWOAs. Coupled with the enhancement in LMWOA exudation rates, root metabolism intensities, measured as the dehydrogenase activity, increased. In contrast, after 40 days of exposure, the exudation rate of total LMWOAs had dropped markedly in PAH-contaminated groups compared to the control, indicating that PAHs negatively impacted root metabolism and activities due to their toxicity. The largest decrease was also found in oxalic acid, suggesting that the biological reactions related with oxalic acid are vulnerable under PAH stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  Google Scholar 

  • Bayen S (2012) Occurrence, bioavailability and toxic effects of trace metals and organic contaminants in mangrove ecosystems: a review. Environ Int 48:84–101

    Article  CAS  Google Scholar 

  • Bhaskaran J, Panneerselvam R (2013) Accelerated reactive oxygen scavenging system and membrane integrity of two Panicum species varying in salt tolerance cell. Biochemistry Biophysics 67:885–892

    Article  CAS  Google Scholar 

  • Chen J, Zhou HC, Wang C, Zhu CQ, Tam NFY (2015) Short-term enhancement effect of nitrogen addition on microbial degradation and plant uptake of polybrominated diphenyl ethers (PBDEs) in contaminated mangrove soil. J Hazard Mater 300:84–92

    Article  CAS  Google Scholar 

  • Chow PS, Landhäusser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136

    Article  CAS  Google Scholar 

  • Chroma L, Mackova M, Kucerova P, Burkhard J, Macek T (2002) Enzymes in plant metabolism of PCBs and PAHs. Acta Biotechnol 22:35–41

    Article  CAS  Google Scholar 

  • Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal-stabilized soil organic matter–the unbutton model. Soil Biol Biochem 84:168–176

    Article  CAS  Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, Amrani AE (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  Google Scholar 

  • Cronan JE Jr, Laporte D (2006) Tricarboxylic acid cycle and glyoxylate bypass. EcoSal Plus 1:206–216

    Google Scholar 

  • Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti nod factors. Science 256:998–1000

    Article  CAS  Google Scholar 

  • Feller I, Lovelock C, Berger U, McKee K, Joye S, Ball M (2010) Biocomplexity in mangrove ecosystems. Annu Rev Mar Sci 2:395–417

    Article  CAS  Google Scholar 

  • Fismes J, Perrin-Ganier C, Empereur-Bissonnet P, Morel JL (2002) Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. J. Environ Qual 31:1649–1656

    Article  CAS  Google Scholar 

  • Gan S, Lau E, Ng H (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549

    Article  CAS  Google Scholar 

  • Gao Y, Yuan X, Lin X, Sun B, Zhao Z (2015) Low-molecular-weight organic acids enhance the release of bound PAH residues in soils. Soil Tillage Res 145:103–110

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular California Agricultural Experiment Station 347:2–32

    Google Scholar 

  • Huang G, Guo G, Yao S, Zhang N, Hu H (2016) Organic acids, amino acids compositions in the root exudates and cu-accumulation in castor (Ricinus communis L.) under cu stress. Int J Phytorem 18:33–40

    Article  Google Scholar 

  • Jia H, Lu H, Liu J, Li J, Dai M, Yan C (2016a) Effects of root exudates on the leachability, distribution, and bioavailability of phenanthrene and pyrene from mangrove sediments. Environ Sci Pollut Res 23:5566–5576

    Article  CAS  Google Scholar 

  • Jia H, Wang H, Lu H, Jiang S, Dai M, Liu J, Yan C (2016b) Rhizodegradation potential and tolerance of Avicennia marina (Forsk.) Vierh in phenanthrene and pyrene contaminated sediments. Mar Pollut Bull 110:112–118

    Article  CAS  Google Scholar 

  • Jiang S, Lu H, Zhang Q, Liu J, Yan C (2016) Effect of enhanced reactive nitrogen availability on plant-sediment mediated degradation of polycyclic aromatic hydrocarbons in contaminated mangrove sediment. Mar Pollut Bull 110:424–431

    Article  CAS  Google Scholar 

  • Kang F, Chen D, Gao Y, Zhang Y (2010) Distribution of polycyclic aromatic hydrocarbons in subcellular root tissues of ryegrass (Lolium multiflorum lam.) BMC Plant Biol 10:1–7

    Article  Google Scholar 

  • Keiluweit M, Bougoure JJ, Nico PS, Pettridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595

    Article  CAS  Google Scholar 

  • Lee SY et al (2014) Ecological role and services of tropical mangrove ecosystems: a reassessment. Global Ecology Biogeography 23:726–743

    Article  Google Scholar 

  • Li G, Wan S, Zhou J, Yang Z, Qin P (2010) Leaf chlorophyll fluorescence, hyperspectral reflectance, pigments content, malondialdehyde and proline accumulation responses of castor bean (Ricinus communis L.) seedlings to salt stress levels. Ind Crop Prod 31:13–19

    Article  Google Scholar 

  • Li R, Zhu Y, Zhang Y (2015) In situ investigation of the mechanisms of the transport to tissues of polycyclic aromatic hydrocarbons adsorbed onto the root surface of Kandelia obovata seedlings. Environ Pollut 201:100–106

    Article  CAS  Google Scholar 

  • Liu W, Hou J, Wang Q, Yang H, Luo Y, Christie P (2015) Collection and analysis of root exudates of Festuca arundinacea L. and their role in facilitating the phytoremediation of petroleum-contaminated soil. Plant Soil 389:109–119

    Article  CAS  Google Scholar 

  • Lu H, Yan C, Liu J (2007) Low-molecular-weight organic acids exuded by mangrove (Kandelia candel (L.) Druce) roots and their effect on cadmium species change in the rhizosphere. Environ Exp Bot 61:159–166

    Article  CAS  Google Scholar 

  • Lu H, Zhang Y, Liu B, Liu J, Ye J, Yan C (2011) Rhizodegradation gradients of phenanthrene and pyrene in sediment of mangrove (Kandelia candel (L.) Druce). J Hazard Mater 196:263–269

    Article  CAS  Google Scholar 

  • 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 162:413–421

    Article  CAS  Google Scholar 

  • Martin BC, George SJ, Price CA, Ryan MH, Tibbett M (2014) The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci Total Environ 472:642–653

    Article  CAS  Google Scholar 

  • Martin BC, George SJ, Price CA, Shahsavari E, Ball AS, Tibbett M, Ryan MH (2016) Citrate and malonate increase microbial activity and alter microbial community composition in uncontaminated and diesel-contaminated soil microcosms. Soil 2:487–498

    Article  Google Scholar 

  • Moermond CT, Traas TP, Roessink I, Veltman K, Hendriks AJ, Koelmans AA (2007) Modeling decreased food chain accumulation of PAHs due to strong sorption to carbonaceous materials and metabolic transformation. Environ Sci Technol 41:6185–6191

    Article  CAS  Google Scholar 

  • Morton JF (1965) Can the red mangrove provide food, feed and fertilizer? Econ Bot 19:113–123

    Article  CAS  Google Scholar 

  • Sukhdhane K, Pandey P, Vennila A, Purushothaman C, Ajima M (2015) Sources, distribution and risk assessment of polycyclic aromatic hydrocarbons in the mangrove sediments of Thane Creek, Maharashtra, India. Environ Monit Assess 187:1–14

    Article  CAS  Google Scholar 

  • Sun T, Cang L, Wang Q, Zhou D, Cheng J, Xu H (2010) Roles of abiotic losses, microbes, plant roots, and root exudates on phytoremediation of PAHs in a barren soil. J Hazard Mater 176:919–925

    Article  CAS  Google Scholar 

  • Suriyagoda LDB, Lambers H, Renton M, Ryan MH (2012) Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply. Plant Soil 358:105–117

    Article  CAS  Google Scholar 

  • Técher D, Laval-Gilly P, Henry S, Bennasroune A, Formanek P, Martinez-Chois C, D'Innocenzo M, Muanda F, Dicko A, Rejšek K, Falla J (2011) Contribution of Miscanthus x giganteus root exudates to the biostimulation of PAH degradation: an in vitro study. Sci Total Environ 409:4489–4495

    Article  Google Scholar 

  • Wang Y, Fang L, Lin L, Luan T, Tam NF (2014) Effects of low molecular-weight organic acids and dehydrogenase activity in rhizosphere sediments of mangrove plants on phytoremediation of polycyclic aromatic hydrocarbons. Chemosphere 99:152–159

    Article  CAS  Google Scholar 

  • Xiao M, Wu F (2014) A review of environmental characteristics and effects of low-molecular weight organic acids in the surface ecosystem. J Environ Sci 26:935–954

    Article  CAS  Google Scholar 

  • Xie M, Yan C, Ye J, Wei L (2009) Impact of phenanthrene on organic acids secretion and accumulation by perennial ryegrass, Lolium perenne L., root. Bull Environ Contam Toxicol 83:75–80

    Article  CAS  Google Scholar 

  • Xie X, Weiss DJ, Weng B, Liu J, Lu H, Yan C (2013) The short-term effect of cadmium on low molecular weight organic acid and amino acid exudation from mangrove (Kandelia obovata (S., L.) Yong) roots. Environ Sci Pollut Res 20:997–1008

    Article  CAS  Google Scholar 

  • Yu K, Wong A, Yau K, Wong Y, Tam N (2005) Natural attenuation, biostimulation and bioaugmentation on biodegradation of polycyclic aromatic hydrocarbons (PAHs) in mangrove sediments. Mar Pollut Bull 51:1071–1077

    Article  CAS  Google Scholar 

  • Zhan X, Liang X, Xu G, Zhou L (2013) Influence of plant root morphology and tissue composition on phenanthrene uptake: stepwise multiple linear regression analysis. Environ Pollut 179:294–300

    Article  CAS  Google Scholar 

  • Zhan X, Yuan J, Yue L, Xu G, Hu B, Xu R (2015) Response of uptake and translocation of phenanthrene to nitrogen form in lettuce and wheat seedlings. Environ Sci Pollut Res 22:6280–6287

    Article  CAS  Google Scholar 

  • Zhao Z, Chu Y, Gu J (2012) Distribution and sources of polycyclic aromatic hydrocarbons in sediments of the Mai Po inner deep Bay Ramsar site in Hong Kong. Ecotoxicology 21:1743–1752

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (31530008), Ministry of Science and Technology of the People’s Republic of China (2013CB956504) and National Natural Science Foundation of China (31370516). The authors would like to thank Ms. Jing Ye, Mr. Yang Bai, Dr. Jingna Du, Dr. Xiangyu Xie, Dr. Jingna Du, and Dr. Bosen Weng for the assistance in field campaigns and laboratory analyses. We also appreciate Dr. Tara Kelly at Trinity College Dublin for the grammar polishing. Thanks are also due to the anonymous reviewers and the editor, whose comments helped to improve the original manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen, 361005, China

    Shan Jiang, Feng Xie, Haoliang Lu, Jingchun Liu & Chongling Yan

Authors
  1. Shan Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Feng Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haoliang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jingchun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chongling Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chongling Yan.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, S., Xie, F., Lu, H. et al. Response of low-molecular-weight organic acids in mangrove root exudates to exposure of polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 24, 12484–12493 (2017). https://doi.org/10.1007/s11356-017-8845-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8845-4

Keywords

Search

Navigation