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The role of laccase in stabilization of soil organic matter by iron in various plant-dominated peatlands: degradation or sequestration?

  • Yunpeng Zhao
  • Wu XiangEmail author
  • Ming Ma
  • Xiuzhi Zhang
  • Zhengyu Bao
  • Shuyun Xie
  • Sen Yan
Regular Article
  • 40 Downloads

Abstract

Aims

The association of organic matter with iron (Fe-OM associations) is recognized as an important stabilization mechanism for soil organic matter. Our objective was to assess the factors regulating stabilization of soil organic matter by iron in various plant-dominated peatlands, and the role of laccase in the formation of Fe-OM associations.

Methods

We investigated Fe-bound OC content and related physicochemical and biochemical parameters in four plots with different successional vegetation, and a set of simulations was conducted to investigate the association of Fe and peat-derived dissolved organic carbon catalysed by laccase.

Results

Our results indicate Fe-bound OC content varies regularly with the succession gradients, and a significant positive relationship between laccase activities and Fe-bound OC content was found (R = 0.77, P < 0.05). Although laccase degradation of recalcitrant polyphenolics is related with the CO2 release from peat soils (R = 0.697; P < 0.05), the simulation results confirmed laccase can significantly promote the formation of Fe-OM association.

Conclusions

We propose that laccase plays a unique multifunctional role in the peatland carbon cycle. That is, while laccase degrades refractory organic matter such as lignin, it may enhance carbon sequestration by promoting the formation of Fe-OM association, which is particularly effective in acidic peat environments containing abundant iron and laccase-producing fungi.

Keywords

Peatland Carbon cycle Soil organic matter Fe-OM associations Laccase Stabilization 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC 41472316), the Hebei Provincial Department of Finance (2121299) and the Fundamental Research Funds for the Central University (CUG170104). We also thank the anonymous reviewers for their valuable suggestions.

References

  1. Ashworth DJ, Shaw G (2006) Effects of moisture content and redox potential on in situ Kd values for radioiodine in soil. Sci Total Environ 359:244–254CrossRefGoogle Scholar
  2. Ausec L, van Elsas JD, Mandicmulec I (2011) Two-and three domain bacterial laccase-like genes are present in drained peat soils. Soil Biol Biochem 43:975–983CrossRefGoogle Scholar
  3. Bhattacharyya A, Schmidt MP, Stavitski E, Martínez CE (2018) Iron speciation in peats: chemical and spectroscopic evidence for the co-occurrence of ferric and ferrous iron in organic complexes and mineral precipitates. Org Geochem 115:124–137CrossRefGoogle Scholar
  4. Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc Natl Acad Sci 108:19473–19481CrossRefGoogle Scholar
  5. Box JD (1983) Investigation of the folin-ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17:249–261CrossRefGoogle Scholar
  6. Bragazza L, Parisod J, Buttler A et al (2012) Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands. Nat Clim Chang 3:273–277CrossRefGoogle Scholar
  7. Chiapusio G, Jassey VEJ, Bellvert F, Comte G, Weston LA, Delarue F, Buttler A, Toussaint ML, Binet P (2018) Sphagnum species modulate their phenolic profiles and mycorrhizal colonization of surrounding Andromeda polifolia along peatland microhabitat. J Chem Ecol 44:1146–1157CrossRefGoogle Scholar
  8. Christl I, Kretzschmar R (2007) C-1s NEXAFS spectroscopy reveals chemical fractionation of humic acid by cation-induced coagulation. Environ Sci Technol 41:1915–1920CrossRefGoogle Scholar
  9. Fellman JB, Hood E, Spencer RGM (2010) Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: a review. Limnol Oceanogr 55:2452–2462CrossRefGoogle Scholar
  10. Feng Y, Colosi LM, Gao S, Huang Q, Mao L (2013) Transformation and removal of Tetrabromobisphenol a from water in the presence of natural organic matter via laccase-catalyzed reactions: reaction rates, products, and pathways. Environ Sci Technol 47:1001–1008CrossRefGoogle Scholar
  11. Fenner N, Freeman C (2011) Drought-induced carbon loss in peatlands. Nat Geosci 4:895–900CrossRefGoogle Scholar
  12. Fenner N, Freeman C, Reynolds B (2004) Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes: implications for the global carbon cycle and soil enzyme methodologies. Soil Biol Biochem 37:1814–1821CrossRefGoogle Scholar
  13. Freeman C, Ostle N, Kang H (2001) An enzymatic ‘latch’ on a global carbon store. Nature 409:149CrossRefGoogle Scholar
  14. Garg S, Jiang C, Waite TD (2018) Impact of pH on Iron redox transformations in simulated freshwaters containing natural organic matter. Environ Sci Technol 52:13184–13194CrossRefGoogle Scholar
  15. Huang X, Xue J, Wang X, Meyers PA, Huang J, Xie S (2013) Paleoclimate influence on early diagenesis of plant triterpenes in the Dajiuhu peatland, Central China. Geochim Cosmochim Acta 123:106–119CrossRefGoogle Scholar
  16. Huber D, Ortner A, Daxbacher A, Nyanhongo GS, Bauer W, Guebitz GM (2016) Influence of oxygen and mediators on laccase catalyzed polymerization of lignosulfonate. ACS Sustain Chem Eng 4:5303–5310CrossRefGoogle Scholar
  17. Jassey VEJ, Chiapusio G, Binet B (2013) Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions. Glob Biol Chang 19:811–823CrossRefGoogle Scholar
  18. Kang H, Kwon MJ, Kim S et al (2018) Biologically driven DOC release from peatlands during recovery from acidification. Nat Commun 9:1–7CrossRefGoogle Scholar
  19. Kellner H, Luis P, Zimdars B, Kiesel B, Buscot F (2008) Diversity of bacterial laccase-like multicopper oxidase genes in forest and grassland Cambisoil soil samples. Soil Biol Biochem 40:638–648CrossRefGoogle Scholar
  20. Kleber M, Mikutta R, Torn MS (2005) Poorly crystalline mineral phases protect organic matter in acid subsoil horizons. Eur J Soil Sci 56:717–725Google Scholar
  21. Kleber M, Eusterhues K, Keiluweit K et al (2015) Mineral–organic associations: formation, properties, and relevance in soil. Adv Agron 130:1–140CrossRefGoogle Scholar
  22. Lalonde K, Mucci A, Ouellet A (2012) Preservation of organic matter in sediments promoted by iron. Nature 483:198–200CrossRefGoogle Scholar
  23. Leonowicz A, Edgehill RU, Bollag JM (1984) The effect of pH on the transformation of syringic and vanillic acids by the laccases of Rhizoctonia praticola and Trametes versicolor. Arch Microbiol 137:89–96CrossRefGoogle Scholar
  24. Li Y, Ma C, Zhou B, Cui A, Zhu C, Huang R, Zheng C (2016) Environmental processes derived from peatland geochemistry since the last deglaciation in Dajiuhu, Shennongjia, Central China. Boreas 45:423–438CrossRefGoogle Scholar
  25. Li X, Yao ST, Dang N et al (2017) The research progress on laccase biotransformation phenolic compound. Adv Microbiol 6:79–89Google Scholar
  26. Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A (2014) The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol 12:797–808CrossRefGoogle Scholar
  27. Mikutta R, Lorenz D, Guggenberger G, Haumaier L, Freund A (2014) Properties and reactivity of Fe-organic matter associations formed by coprecipitation versus adsorption: clues from arsenate batch adsorption. Geochim Cosmochim Acta 144:258–276CrossRefGoogle Scholar
  28. Murphy EM, Zachara JM, Smith SC (1990) Influence of mineral-bound humic substances on the sorption of hydrophobic organic compounds. Environ Sci Technol 24:1507–1516CrossRefGoogle Scholar
  29. O'Loughlin EJ (2008) Effects of Electron transfer mediators on the bioreduction of Lepidocrocite (γ-FeOOH) by Shewanella putrefaciens CN32. Environ Sci Technol 42:6876–6882CrossRefGoogle Scholar
  30. Poggenburg C, Mikutta R, Sander M, Schippers A, Marchanka A, Dohrmann R, Guggenberger G (2016) Microbial reduction of ferrihydrite-organic matter coprecipitates by Shewanella putrefaciens and Geobacter metallireducens in comparison to mediated electrochemical reduction. Chem Geol 447:133–147CrossRefGoogle Scholar
  31. Potvin LR, Kane ES, Chimner RA, Kolka RK, Lilleskov EA (2015) Effects of water table position and plant functional group on plant community, aboveground production, and peat properties in a peatland mesocosm experiment (PEATcosm). Plant Soil 387:277–294CrossRefGoogle Scholar
  32. Raiswell R, Canfield DE (2012) The iron biogeochemical cycle past and present. Geochem Perspect 1:1–220CrossRefGoogle Scholar
  33. Rezanezhad F, Price JS, Quinton WL, Lennartz B, Milojevic T, van Cappellen P (2016) Structure of peat soils and implications for water storage, flow and solute transport: a review update for geochemists. Chem Geol 429:75–84CrossRefGoogle Scholar
  34. Ricklefs E, Winkler N, Koschorreck K, Urlacher VB (2014) Expanding the laccase-toolbox: a laccase from Corynebacterium glutamicum with phenol coupling and cuprous oxidase activity. J Biotechnol 191:46–53CrossRefGoogle Scholar
  35. Riedel T, Zak D, Biester H, Dittmar T (2013) Iron traps terrestrially derived dissolved organic matter at redox interfaces. Proc Natl Acad Sci 110:10101–10105CrossRefGoogle Scholar
  36. Robroek BJM, Albrecht RJH, Hamard S et al (2015) Peatland vascular plant functional types affect dissolved organic matter chemistry. Plant Soil 407:135–143CrossRefGoogle Scholar
  37. Saraswati S, Parsons CT, Strack M (2019) Access roads impact enzyme activities in boreal forested peatlands. Sci Total Environ 651:1405–1415CrossRefGoogle Scholar
  38. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  39. Straková P, Anttila J, Spetz P, Kitunen V, Tapanila T, Laiho R (2010) Litter quality and its response to water level drawdown in boreal peatlands at plant species and community level. Plant Soil 335:501–520CrossRefGoogle Scholar
  40. Štursová M, Baldrian P (2011) Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity. Plant Soil 338:99–110CrossRefGoogle Scholar
  41. Theuerl S, Buscot F (2010) Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biol Fertil Soils 46:215–225CrossRefGoogle Scholar
  42. Thompson A, Chadwick OA, Rancourt DG (2006) Iron-oxide crystallinity increases during soil redox oscillations. Geochim Cosmochim Acta 70:1710–1727CrossRefGoogle Scholar
  43. Varadachari C, Ghosh K (1984) On humus formation. Plant Soil 77:305–313CrossRefGoogle Scholar
  44. Wagai R, Mayer LM (2007) Sportive stabilization of organic matter in soils by hydrous iron oxides. Geochim Cosmochim Acta 71:25–35CrossRefGoogle Scholar
  45. Wang Y, Wang H, He JS, Feng X (2017) Iron-mediated soil carbon response to water-table decline in an alpine wetland. Nat Commun 8:15972CrossRefGoogle Scholar
  46. Xiang W, Wan X, Yan S, Wu Y, Bao Z (2013) Inhibitory effects of drought induced acidification on phenol oxidase activities in Sphagnum-dominated peatland. Biogeochemistry 116:293–301CrossRefGoogle Scholar
  47. Yin Y, Wang Y, Li S et al (2019) Soil microbial character response to plant community variation after grazing prohibition for 10 years in a Qinghai-Tibetan alpine meadow. Plant Soil 436:1–15CrossRefGoogle Scholar
  48. Zhao Q, Adhikari D, Huang R, Patel A, Wang X, Tang Y, Obrist D, Roden EE, Yang Y (2017) Coupled dynamics of iron and iron-bound organic carbon in forest soils during anaerobic reduction. Chem Geol 464:118–126CrossRefGoogle Scholar
  49. Zhao YP, Xiang W, Yan S, Huang Y, Fan W (2019) Laccase activity in Sphagnum-dominated peatland: a study based on a novel measurement of delay dynamics (MDD) for determining laccase activity. Soil Biol Biochem 133:108–115CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Yunpeng Zhao
    • 1
  • Wu Xiang
    • 1
    Email author
  • Ming Ma
    • 2
  • Xiuzhi Zhang
    • 3
  • Zhengyu Bao
    • 2
  • Shuyun Xie
    • 1
  • Sen Yan
    • 1
  1. 1.Hubei Key Laboratory of Critical Zone Evolution, School of Earth SciencesChina University of GeosciencesWuhanPeople’s Republic of China
  2. 2.Zhejiang InstituteChina University of GeosciencesHangzhouChina
  3. 3.Hebei Institute of Geological SurveyShijiazhuangChina

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