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Properties of root exudates and rhizosphere sediment of Bruguiera gymnorrhiza (L.)

  • Sediments, Sec 4 • Sediment-Ecology Interactions • Research Article
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Abstract

Purpose

The rhizosphere plays an important role in promoting the biodegradation and phytoremediation processes of organic pollutants in mangrove sediments; however, the mechanisms behind this interaction remain little understood. We analyzed the properties of root exudates and rhizosphere sediment of Bruguiera gymnorrhiza (L.) to provide basic information about the rhizosphere effects of mangroves.

Materials and methods

We analyzed the organic components and the low-molecular-weight organic acids in root exudates extracted from hydroponic culture solution, and the rhizosphere and non-rhizosphere sediments using gas chromatography-mass spectrometer and high-performance liquid chromatography. A 16S rDNA gene analysis was performed to investigate the bacterial community and diversity of sediments. The sediment organic carbon structures were analyzed using solid-state 13C nuclear magnetic resonance. A stable carbon isotopic analysis was conducted to assess the contribution of root exudates and litter (root, stem, and leaf) to sediment organic matter.

Results and discussion

The organic components in the mangrove root exudates were collected from the hydroponic culture solution sediments and included hydrocarbons, esters, phenols, and aromas in both the rhizosphere and non-rhizosphere sediments. However, the content of each component and the dominant components were different between the rhizosphere and non-rhizosphere sediments. The rhizosphere sediment showed a higher level of organic carbon, nutrient elements, cation exchange capacity, microorganism density, enzyme activities, and bacterial diversity than the non-rhizosphere sediment. Litter is the main organic matter resource of the rhizosphere sediment; however, the rhizosphere sediment also received more labile organic matters from root exudates. In the rhizosphere sediment, the percentage of macroaggregates (>1 mm) and the stability of the physical structure were higher than those of the non-rhizosphere sediment. In addition, the microorganism density and bacterial diversity of macroaggregates was higher than those of mesoaggregates (0.25–1 mm) and microaggregates (<0.25 mm).

Conclusions

As a result of the input of root exudates, the rhizosphere sediment had different chemical, physical, and microbial properties from the non-rhizosphere sediment. The predominant properties of the rhizosphere sediment were high content of organic matters, stable physical structure, and high microbial activity. This comprehensive understanding of the rhizosphere effects of mangroves is crucial for further studying of the promoted biodegradation and phytoremediation of organic pollutants in this special system.

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References

  • Alvarez A, Yanez ML, Benimeli CS, Amoroso MJ (2012) Maize plants (Zea mays) root exudates enhance lindane removal by native Streptomyces strains. Int Biodeter Biodegr 66:14–18

    Article  CAS  Google Scholar 

  • Bei LB, Ping W, Li C, Yong Z (2011) Effects of aging and flooding on sorption of PAHs in mangrove sediment. Fresenius Environ Bull 20:623–630

    CAS  Google Scholar 

  • Bouillon S, Moens T, Dehairs F (2004) Carbon sources supporting benthic mineralization in mangrove and adjacent seagrass sediments (Gazi Bay, Kenya. Biogeosciences 1:71–78

    Article  CAS  Google Scholar 

  • Burken JG, Schnoor JL (1996) Phytoremediation: plant uptake of atrazine and role of root exudates. J Environ Eng - Asce 122:958–963

    Article  Google Scholar 

  • Cocco S, Agnelli A, Gobran GR, Corti G (2013) Changes induced by the roots of Erica arborea L. To create a suitable environment in a soil developed from alkaline and fine-textured marine sediments. Plant Soil 368:297–313

    Article  CAS  Google Scholar 

  • Dinesh R, Srinivasan V, Hamza S, Parthasarathy VA, Aipe KC (2010) Physico-chemical, biochemical and microbial properties of the rhizospheric soils of tree species used as supports for black pepper cultivation in the humid tropics. Geoderma 158:252–258

    Article  CAS  Google Scholar 

  • Elliott ET (1986) Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Sci Soc Am J 50:627–633

    Article  Google Scholar 

  • Fageria NK, Stone LF (2006) Physical, chemical, and biological changes in the rhizosphere and nutrient availability. J plant. Nutrition 29:1327–1356

    CAS  Google Scholar 

  • Ferreira TO, Vidal-Torrado P, Otero XL, Macías F (2007) Are mangrove forest substrates sediments or soils? A case study in southeastern Brazil. Catena 70:79–91

    Article  Google Scholar 

  • He XP, Wang BD, Xie LP, Xin M, Wang W, Wang ZC, Zhang WQ, Wei QS (2016) Effects of tamarisk shrub on physicochemical properties of soil in coastal wetland of the Bohai Sea. Acta Oceanol Sin 35:106–112

    Article  CAS  Google Scholar 

  • Hinsinger P (2011) Biogeochemical, biophysical, and biological processes in the rhizosphere. In: Huang PM, Li Y, Summer ME (eds) Handbook of soil science resource of management and environmental impacts, 2nd edn. CRC Press, Taylor & Francis, pp. 1–30

    Google Scholar 

  • Hinsinger P, Claude P, Tang C, Benoît J (2003) Origins of root mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • Huang PM, Germida JJ (2002) Chemical and biochemical processes in the rhizosphere: metal pollutants. In: Huang PM, Bollag JM, Senesi N (eds) Interactions between soil particles and microorganisms: impact on the terrestrial ecosystem. John Wiley & Sons, New York, pp. 381–438

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Ke L, Wang WQ, Wong TWY, Wong YS, Tam NFY (2003) Removal of pyrene from contaminated sediments by mangrove microcosms. Chemosphere 51:25–34

    Article  CAS  Google Scholar 

  • Krutz LJ, Beyrouty CA, Gentry TJ, Wolf DC, Reynolds CM (2005) Selective enrichment of a pyrene degrader population and enhanced pyrene degradation in Bermuda grass rhizosphere. Biol Fert. Soils 41:359–364

    Google Scholar 

  • Kumar T, Ray S, Brahmachary RL, Ghose M (2009) Preliminary GC-MS analysis of compounds present in the root exudates of three mangrove species. Acta Chromatogr 21:117–125

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–119

    Article  CAS  Google Scholar 

  • Lewis M, Pryor R, Wilking L (2011) Fate and effects of anthropogenic chemicals in mangrove ecosystems: a review. Environ Pollut 159:2328–2346

    Article  CAS  Google Scholar 

  • Li MS, Lee SY (1997) Mangroves of China: a brief review. Forest Ecol Manag 96:241–259

    Article  Google Scholar 

  • Liu YR, Li X, Shen QR, Xu YC (2013) Enzyme activity in water—stable soil aggregates as affected by long-term application of organic manure and chemical fertiliser. Pedosphere 23:111–119

    Article  CAS  Google Scholar 

  • Lu HL, Yan CL, Liu JC (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 HL, Zhang Y, Liu BB, Liu JC, Ye J, Yan CL (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 

  • Luo L, Zhang SZ, Shan XQ, Zhu YG (2006) Oxalate and root exudates enhance the desorption of p,p′-DDT from soils. Chemosphere 63:1273–1279

    Article  CAS  Google Scholar 

  • Macek T, Mackova M, Káš J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18:23–34

    Article  CAS  Google Scholar 

  • Manju MN, Resmi P, Ratheesh Kumar CS, Gireeshkumar TR, Chandramohanakumar N, Joseph M (2016) Biochemical and stable carbon isotope records of mangrove derived organic matter in the sediment cores. Environ Earth Sci 75:565

    Article  Google Scholar 

  • Meng L, Zhu YG (2011) Pyrene biodegradation in an industrial soil exposed to simulated rhizodeposition: how does it affect functional microbial abundance? Environ Sci Technol 45:1579–1585

    Article  CAS  Google Scholar 

  • Mitton FM, Gonzalez M, Pena A, Miglioranza KSB (2012) Effects of amendments on soil availability and phytoremediation potential of aged p,p′-DDT, p,p′-DDE and p,p’-DDD residues by willow plants (Salix sp. J Hazard Mater 203:62–68

    Article  Google Scholar 

  • Moreira ITA, Oliveira OMC, Triguis JA, Queiroz AFS, Ferreira SLC, Martins CMS, Silva ACM, Falcao BA (2013) Phytoremediation in mangrove sediments impacted by persistent total petroleum hydrocarbons (TPH’s) using Avicennia schaueriana. Mar Pollut Bull 67:130–136

    Article  CAS  Google Scholar 

  • Muzuka ANN, Shunula JP (2006) Stable isotope compositions of organic carbon and nitrogen of two mangrove stands along the Tanzanian coastal zone. Estuar Coast Shelf Sci 66:447–458

    Article  CAS  Google Scholar 

  • Page AL (1982) Methods of soil analysis, second edition. ASA Press, New York

    Google Scholar 

  • Parrish ZD, Banks MJ, Schwab AP (2005) Assessment of contaminant lability during phytoremediation of polycyclic aromatic hydrocarbon impacted soil. Environ Pollut 137:187–197

    Article  CAS  Google Scholar 

  • Pérès G, Cluzeau D, Menasseri S, Soussana JF, Bessler H, Engels C, Habekost M, Gleixner G, Weigelt A, Weisser WW, Scheu S, Eisenhauer N (2013) Mechanisms linking plant community properties to soil aggregate stability in an experimental grassland plant diversity gradient. Plant Soil 373:285–299

    Article  Google Scholar 

  • Phillips LA, Greer CW, Farrell RE, Germida JJ (2012) Plant root exudates impact the hydrocarbon degradation potential of a weathered-hydrocarbon contaminated soil. Appl Soil Ecol 52:56–64

    Article  Google Scholar 

  • Piresa ACC, Clearya DFR, Almeidaa A, Cunhaa Â, Dealtryb S, Mendonça-Haglerc LCS, Smallab K, Gomesa NCM (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Appl Environ Microbiol 78:5520–5528

    Article  Google Scholar 

  • Prakash S, Ramasubburayan R, Iyapparaj P, Ahila NK, Ramkumar VS, Palavesam A, Immanuel G, Kannapiran E (2015) Influence of physicochemical and nutritional factors on bacterial diversity in mangrove sediments along the southwest coast of Tamilnadu, India. Environ Monit Assess 187:562

    Article  CAS  Google Scholar 

  • Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356

    Article  CAS  Google Scholar 

  • Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant Soil 338:143–158

    Article  CAS  Google Scholar 

  • Shultz DJ, Calder JA (1976) Organic carbon variations in estuarine sediments. Geochim Cosmochim Acta 40(4):381–385

  • Sokolova TA (2015) Specificity of soil properties in the rhizosphere: analysis of literature data. Eur. Soil Sci 48:968–980

    CAS  Google Scholar 

  • Strobel BW (2001) Influence of vegetation on low-molecular weight carboxylic acids in soil solution—a review. Geoderma 99:169–198

    Article  CAS  Google Scholar 

  • Sun J, Liu J, Yu M, Wang C, Sun Y, Zhang A, Wang T, Lei Z, Jiang G (2013) In vivo metabolism of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) in young whole pumpkin plant. Environ Sci Technol 47:3701–3707

    Article  CAS  Google Scholar 

  • Tam NFY, Wong YS (2008) Effectiveness of bacterial inoculum and mangrove plants on remediation of sediment contaminated with polycyclic aromatic hydrocarbons. Mar Pollut Bull 57:716–726

    Article  CAS  Google Scholar 

  • Traoreâ O, Groleau-renaud V, Plantureux S, Tubeileh A, Bêuf-tremblay V (2000) Effect of root mucilage and modelled root exudates on soil structure. Eur J Soil Sci 51:575–581

    Article  Google Scholar 

  • Turpault MP, Utérano C, Boudot JP, Ranger J (2005) Influence of mature Douglas fir roots on the solid soil phase of the rhizosphere and its solution chemistry. Plant Soil 275:327–336

    Article  CAS  Google Scholar 

  • Violante A, Caporale AG (2015) Biogeochemical processes at soil-root interface. J Soil Sci Plant Nut 15:422–448

    Google Scholar 

  • Wang YN, Wang MK, Zhuang SY, TC T, Chiang KY (2007) Characterization of low-molecular-weight organic acids and organic carbon of Taiwan red cypress, peacock pine, and moso bamboo in a temperate rain forest. Commun Soil Sci Plant Anal 38:77–91

    Article  Google Scholar 

  • Wang Y, Fang L, Lin L, Luan T, Tam NFY (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 

  • Wang HT, JQ S, Zheng TL, Yang XR (2015) Insights into the role of plant on ammonia-oxidizing bacteria and archaea in the mangrove ecosystem. J Soils Sediments 15:1212–1223

    Article  CAS  Google Scholar 

  • Wenger K, Bigler L, Suter MJF, Schonenberger R, Gupta SK, Schulin R (2005) Effect of corn root exudates on the degradation of atrazine and its chlorinated metabolites in soils. J Environ Qual 34:2187–2196

    Article  CAS  Google Scholar 

  • Xu N, Wei M, Wang C, Shi W, Tian FM, Wang XF (2013) Composition of welsh onion (Allium fistulosum L.) root exudates and their allelopathy on cucumber sprouts and Fusarium oxysporum f. sp cucumerinum. Allelopathy J 32:243–256

    Google Scholar 

  • Yang XG, Liu TS, Chen B (2013) GC-MS analysis of rhizosphere-soil extract of salvia miltiorrhiza bge. Chinese agricultural. Science Bulletin 29:173–177

    Google Scholar 

  • Yoshitomi K, Shann J (2001) Corn (Zea mays L.) root exudates and their impact on 14C-pyrene mineralization. Soil Biol Biochem 33:1769–1776

    Article  CAS  Google Scholar 

  • Zhang C, Liu G, Xue S, Song Z (2011) Rhizosphere soil microbial activity under different vegetation types on the Loess Plateau, China. Geoderma 161:115–125

    Article  CAS  Google Scholar 

  • Zhang ZW, Xu XR, Sun YX, Yu S, Chen YS, Peng JX (2014) Heavy metal and organic contaminants in mangrove ecosystems of China: a review. Environ Sci Pollut R 21:11938–11950

    Article  CAS  Google Scholar 

  • Zhao B, He S (2002) Microbial Experiment, 1st edn. Beijing Science Press, Beijing

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41301555) and the Fundamental Research Funds for Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences (no. 2012hzs1J008).

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Correspondence to Beibei Liu or Lixu Peng.

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Responsible editor: Haihan Zhang

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Liu, B., Liu, X., Huo, S. et al. Properties of root exudates and rhizosphere sediment of Bruguiera gymnorrhiza (L.). J Soils Sediments 17, 266–276 (2017). https://doi.org/10.1007/s11368-016-1541-z

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  • DOI: https://doi.org/10.1007/s11368-016-1541-z

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