Skip to main content
SpringerLink
Log in

Structural characteristics of humic-like acid from microbial utilization of lignin involving different mineral types

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

Abstract

This paper determines the impact of two clay minerals (kaolinite and montmorillonite) and three oxides (goethite, δ-MnO2, and bayerite) on the elemental composition and FTIR spectra of humic-like acid (HLA) extracted from microbial-mineral residue formed from the microbial utilization of lignin in liquid shake flask cultivation. Goethite, bayerite, and δ-MnO2 showed higher enrichment capabilities of C and O + S in the HLA than kaolinite and montmorillonite. Goethite showed the highest retention of organic C, followed by bayerite, but kaolinite exhibited the least exchangeability. Kaolinite and montmorillonite enhanced microbial consumption of N, resulting in the absence of N in HLA. A few aliphatic fractions were preferentially gathered on the surfaces of kaolinite and montmorillonite, making the H/C ratios of HLA from the clay mineral treatments higher than those of HLA from the oxide treatments. δ-MnO2 was considered the most effective catalyst for abiotic humification, and goethite and bayerite ranked second and third in this regard. This trend was proportional to their specific surface areas (SSAs). However, comparing the effects of different treatments on the promotion of HLA condensation by relying solely on the SSA of minerals was not sufficient, and other influencing mechanisms had to be considered as well. Additionally, Si–O–Al and Si–O of kaolinite participated in HLA formation, and Si–OH, Si–O, and Si–O–Al of montmorillonite also contributed to this biological process. Fe–O and phenolic –OH of goethite, Mn–O of δ-MnO2, and Al–O of bayerite were all involved in HLA formation through ligand exchange and cation bridges. Lignin was better protected from microbial decomposition by the kaolinite, bayerite, and δ-MnO2 treatments, which caused lignin-like humus (HS) formation. Under the treatments of δ-MnO2, goethite, and bayerite, HLA showed a greater degree of condensation compared to HLA precipitated by kaolinite and montmorillonite. Contributions from Si–O, and Si–O–Al of clay minerals, and Fe–O, Mn–O, and Al–O of oxides were the mechanisms by which minerals catalyzed the formation of HS from lignin.

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

Similar content being viewed by others

References

  • Adani F, Ricca G (2004) The contribution of alkali soluble (humic acid-like) and unhydrolyzed-alkali soluble (core-humic acid-like) fractions extracted from maize plant to the formation of soil humic acid. Chemosphere 56(1):13–22

  • Al-Essa K, Khalili F (2018) Adsorption of humic acid onto Jordanian kaolinite clay: effects of humic acid concentration, pH, and temperature. Sci J Chem 6(1):1–10

    Article  CAS  Google Scholar 

  • Atkinson RJ, Posner AM, Quirk JP (1967) Adsorption of potential determining ions at the ferric oxide-aqueous electrolyte interface. J Phys Chem C 71(3):550–559

    Article  CAS  Google Scholar 

  • Balan E, Blanchard M, Hochepied J, Lazzeri M (2008) Surface modes in the infrared spectrum of hydrous minerals: the OH stretching modes of bayerite. Phys Chem Miner 35(5):279–285

    Article  CAS  Google Scholar 

  • Balcke GU, Kulikova NA, Hesse S, Kopinke F, Perminova IV, Frimmel FH (2002) Adsorption of humic substances onto kaolin clay related to their structural features. Soil Sci Soc Am J 66(6):1805–1812

    Article  CAS  Google Scholar 

  • Baldock JA, Skjemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31(7-8):697–710

    Article  CAS  Google Scholar 

  • Bolan NS, Kunhikrishnan A, Choppala GK, Thangarajan R, Chung JW (2012) Stabilization of carbon in composts and biochars in relation to carbon sequestration and soil fertility. Sci Total Environ 424(1):264–270

    Article  CAS  Google Scholar 

  • Brunetti G, Senesi N, Plaza C (2008) Organic matter humification in olive oil mill wastewater by abiotic catalysis with manganese (IV) oxide. Bioresource Technal 99(17):8528–8531

    Article  CAS  Google Scholar 

  • Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28(12):1883–1896

    Article  CAS  Google Scholar 

  • Campitelli P, Ceppi S (2008) Effects of composting technologies on the chemical and physicochemical properties of humic acids. Geoderma 144(1-2):325–333

    Article  CAS  Google Scholar 

  • Campos B, Aguilar-Carrillo J, Algarra M, Gonçalves MA, Rodríguez-Castellón E, Esteves da Silva JCG, Bobos I (2013) Adsorption of uranyl ions on kaolinite, montmorillonite, humic acid and composite clay material. Appl Clay Sci 85:53–63

  • Chen YM, Tsao TM, Liu CC, Huang PM, Wang MK (2010) Polymerization of catechin catalyzed by Mn-, Fe- and Al-oxides. Colloids Surf B Biointerfaces 81(1):217–223

    Article  Google Scholar 

  • Chenu C (1995) Extracellular polysaccharides: an interface between microorganisms and soil constituents. In: Huang PM, Berthelin J, Bollag JM, McGill WB, Page AL (eds) Environmental impact of soil component interactions: natural and anthropogenic organics. CRC Press, Boca Raton, pp 217–233

    Google Scholar 

  • Chorover J, Amistadi MK (2001) Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim Cosmochim Ac 65(1):95–109

    Article  CAS  Google Scholar 

  • Conte P, Abbate C, Baglieri A, Nègre M, Pasquale CD, Alonzo G, Gennari M (2011) Adsorption of dissolved organic matter on clay minerals as assessed by infra-red, CPMAS 13C NMR spectroscopy and low field T 1 NMR relaxometry. Org Geochem 42(8):972–977

  • Cui TT, Li ZH, Wang SJ (2017) Effects of in-situ straw decomposition on composition of humus and structure of humic acid at different soil depths. J Soil Sediment 17(10):2391–2399

    Article  CAS  Google Scholar 

  • Feng XJ, Simpson AJ, Simpson MJ (2005) Chemical and mineralogical controls on humic acid sorption to clay mineral surfaces. Org Geochem 36(11):1553–1566

    Article  CAS  Google Scholar 

  • Fleury G, Nero MD, Barillon R (2017) Effect of mineral surface properties (alumina, kaolinite) on the sorptive fractionation mechanisms of soil fulvic acids: Molecular-scale ESI-MS studies. Geochim Cosmochim Ac 196(1):1–17

    Article  CAS  Google Scholar 

  • Fu HB, Quan X (2006) Complexes of fulvic acid on the surface of hematite, goethite, and akaganeite: FTIR observation. Chemosphere 63(3):403–410

  • Fukuchi S, Miura A, Okabe R, Fukushima M, Sasaki M, Sato T (2010) Spectroscopic investigations of humic-like acids formed via polycondensation reactions between glycine, catechol and glucose in the presence of natural zeolites. J Mol Struct 982(1–3):181–186

    Article  CAS  Google Scholar 

  • Gao XT, Tan WB, Zhao Y, Wu JQ, Sun QH, Qi HS, Xie XY, Wei ZM (2019) Diversity in the mechanisms of humin formation during composting with different materials. Environ Sci Technol 53:3653–3662

    Article  CAS  Google Scholar 

  • Ghabbour EA, Davies G (2001) Humic substances: structures, models and functions. Royal Soc Chem (Chapter 4)

  • Ghosh S, Wang ZY, Kang S, Bhowmik PC, Xing BS (2009) Sorption and fractionation of a peat derived humic acid by kaolinite, montmorillonite, and goethite. Pedosphere 19(1):21–30

    Article  CAS  Google Scholar 

  • Gonzalez JM (2002) Role of clay minerals on soil organic matter stabilization and humification. Iowa State University, Iowa State University Capstones, Theses and Dissertations

  • Hardie AG, Dynes JJ, Kozak LM, Huang PM (2010) Abiotic catalysis of the Maillard reaction and polyphenol-Maillard humification pathways by Al, Fe and Mn oxides. 19th World Congress of Soil Science, 9–12

  • Hennig E (2016) Secrets of fertile soils: humus as the guardian of the fundamentals of natural life. Chapter 2. Acres USA Inc, Texas

  • Hizal J, Apak R (2006a) Modeling of cadmium (II) adsorption on kaolinite-based clays in the absence and presence of humic acid. Appl Clay Sci 32(3–4):232–244

    Article  CAS  Google Scholar 

  • Hizal J, Apak R (2006b) Modeling of copper(II) and lead(II) adsorption on kaolinite-based clay minerals individually and in the presence of humic acid. J Colloid Interf Sci 295(1):1–13

    Article  CAS  Google Scholar 

  • Huang PM, Wang MK, Chiu CY (2005) Soil mineral–organic matter–microbe interactions: Impacts on biogeochemical processes and biodiversity in soils. Pedobiologia 49(6):609–635

    Article  CAS  Google Scholar 

  • Huang DL, Zeng GM, Huang GH, Hu TJ, Jiang XY, Feng CL, Chen YN (2006) Application of white-rot fungi in composting lead contaminated waste. Environmental Science 27(1):175–180 In Chinese

    CAS  Google Scholar 

  • Hur J, Schlautman MA (2003) Molecular weight fractionation of humic substances by adsorption onto minerals. J Colloid Interf Sci 264(2):313–321

    Article  CAS  Google Scholar 

  • Ingrid KK (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34(2):139–162

    Article  Google Scholar 

  • Janusz G, Pawlik A, Sulej J, Świderska-Burek U, Jarosz-Wilkołazka A, Paszczyński A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41(6):941–962

    Article  CAS  Google Scholar 

  • Jayarathna L, Makehelwala M, Bandara A, Weerasooriya R (2018) Vibration spectroscopic evidence for different interactive modes of iodide on gibbsite in humic acid mediation. Colloid Polym Sci 296(7):1259–1265

    Article  CAS  Google Scholar 

  • Jokic A, Frenkel AI, Vairavamurthy MA, Huang PM (2001) Birnessite catalysis of the Maillard reaction: its significance in natural humification. Geophys Res Lett 28(20):3899–3902

    Article  CAS  Google Scholar 

  • Joseph C, Stockmann M, Schmeide K, Sachs S, Brendler V, Bernhard G (2013) Sorption of U(VI) onto opalinus clay: effects of pH and humic acid. Appl Geochem 36:104–117

    Article  CAS  Google Scholar 

  • Karpukhina E, Mikheev I, Perminova I, Volkov D, Proskurnin M (2018) Rapid quantification of humic components in concentrated humate fertilizer solutions by FTIR spectroscopy. J Soil Sediment 19:2729–2739. https://doi.org/10.1007/s11368-018-2133-x

    Article  CAS  Google Scholar 

  • Kaur N, Kishore D (2012) Montmorillonite: an efficient, heterogeneous and green catalyst for organic synthesis. J Chem Pharm Res 4(2):991–1015

    CAS  Google Scholar 

  • Kögel-Knabner I, Kleber M (2011) Mineralogical physicochemical and microbiological controls on soil organic matter stabilization and turnover. In: Huang PM, Li Y, Sumner ME (eds) Handbook of Soil Sciences. CRC Press, Boca Raton, pp 7–22

    Google Scholar 

  • Majzik A, Tombácz E (2007) Interaction between humic acid and montmorillonite in the presence of calcium ions I. Interfacial and aqueous phase equilibria: Adsorption and complexation. Org Geochem 38(8):1319–1329

    Article  CAS  Google Scholar 

  • Mak MS, Lo IM (2011) Influences of redox transformation, metal complexation and aggregation of fulvic acid and humic acid on Cr(VI) and As(V) removal by zero-valent iron. Chemosphere 84(2):234–240

    Article  CAS  Google Scholar 

  • Martin JP, Filip Z, Haider K (1976) Effect of montmorillonite and humate on growth and metabolic activity of some actinomycetes. Soil Biol Biochem 8(5):409–413

    Article  CAS  Google Scholar 

  • Martinez RE, Sharma P, Kappler A (2010) Surface binding site analysis of Ca2+–homoionized clay–humic acid complexes. J Colloid Interf Sci 352(2):526–534

  • Marumoto T, Anderson JPE, Domsch KH (1982) Mineralization of nutrients from soil microbial biomass. Soil Biol Biochem 14(5):469–475

    Article  CAS  Google Scholar 

  • Medina J, Monreal C, Chabot D, Meier S, González ME, Morales E, Parillo R, Borie F, Cornejo P (2017) Microscopic and spectroscopic characterization of humic substances from a compost amended copper contaminated soil: main features and their potential effects on Cu immobilization. Environ Sci Pollut R 24(16):14104–14116

    Article  CAS  Google Scholar 

  • Mitchell PJ, Simpson AJ, Soong R, Simpson MJ (2018) Nuclear magnetic resonance analysis of changes in dissolved organic matter composition with successive layering on clay mineral surfaces. Soil Syst 2(1):8

    Article  CAS  Google Scholar 

  • Miura A, Fukuchi S, Okabe R, Fukushima M, Sasaki M, Sato T (2011) Effect of different fractions of weathered pumice in the formation of humic-like substances. Clay Miner 46(4):637–648

    Article  CAS  Google Scholar 

  • Namita D, Natarajan KA, Somasundaran P (2001) Mechanisms of adhesion of Paenibacillus polymyxa onto hematite, corundum and quartz. Int J Miner Process 62(1–4):27–39

    Google Scholar 

  • Namjesnik-Dejanovic K, Maurice PA, Aiken GR, Cabaniss S, Chin YP, Pullin MJ (2000) Adsorption and fractionation of a muck fulvic acid on kaolinite and goethite at pH 3.7, 6, and 8. Soil Sci 165(7):545–559

    Article  CAS  Google Scholar 

  • Nishimoto R, Fukuchi S, Qi GX, Fukushima M, Sato T (2013) Effects of surface Fe(III) oxides in a steel slag on the formation of humic-like dark-colored polymers by the polycondensation of humic precursors. Colloid Surf A-Physicochem Eng Asp 418(5):117–123

    Article  CAS  Google Scholar 

  • Palanivell P, Susilawati K, Ahmed OH, Majid NM (2013) Compost and crude humic substances produced from selected wastes and their effects on Zea mays L. nutrient uptake and growth. Sci World J 2013:1–15

    Article  Google Scholar 

  • Pinskiy D, Maltseva A, Zolotareva B (2014) Role of mineral matrix composition and properties in the transformation of corn residues. Eur J Soil Sci 3:172–181

    Google Scholar 

  • Qi GX, Yue DB, Fukushima M, Fukuchi S, Nie YF (2012) Enhanced humification by carbonated basic oxygen furnace steel slag-I. Characterization of humic-like acids produced from humic precursors. Bioresour Technol 104:497–502

    Article  CAS  Google Scholar 

  • Qin XP, Liu F, Wang GC, Hou H, Li FS, Weng LP (2015) Fractionation of humic acid upon adsorption to goethite: Batch and column studies. Chem Eng J 269:272–278

    Article  CAS  Google Scholar 

  • Rakhsh F, Golchin A, Agha ABA, Alamdari P (2017) Effects of exchangeable cations, mineralogy and clay content on the mineralization of plant residue carbon. Geoderma 307(1):150–158

    Article  CAS  Google Scholar 

  • Rao MA, Russo F, Granata V, Berisio R, Zagari A, Gianfreda L (2007) Fate of prions in soil: Interaction of a recombinant ovine prion protein with synthetic humic-like mineral complexes. Soil Biol Biochem 39(2):493–504

  • Rong XM, Huang QY, Chen WL (2007) Microcalorimetric investigation on the metabolic activity of Bacillus thuringiensis as influenced by kaolinite, montmorillonite and goethite. Appl Clay Sci 38(1–2):97–103

    Article  CAS  Google Scholar 

  • Shindo H (1992) Relative effectiveness of short-range ordered Mn(IV), Fe(III), Al, and Si oxides in the synthesis of humic acids from phenolic compounds. Soil Sci Plant Nutr 38(3):459–465

    Article  CAS  Google Scholar 

  • Singh M, Sarkar B, Biswas B, Churchman J, Bolan NS (2016) Adsorption-desorption behavior of dissolved organic carbon by soil clay fractions of varying mineralogy. Geoderma 280(15):47–56

    Article  CAS  Google Scholar 

  • Supanchaiyamat N, Jetsrisuparb K, Knijnenburg JTN, Tsang DCW, Hunt AJ (2018) Lignin materials for adsorption: current trend, perspectives and opportunities. Bioresour Technol 272:570–581. https://doi.org/10.1016/j.biortech.2018.09.139

    Article  CAS  Google Scholar 

  • Thevenot M, Dignac MF, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42(8):1200–1211

    Article  CAS  Google Scholar 

  • Trompowsky PM, Benites VDM, Madari BE, Pimenta AS, Hockaday WC, Hatcher PG (2005) Characterization of humic like substances obtained by chemical oxidation of eucalyptus charcoal. Org Geochem 36(11):1480–1489

    Article  CAS  Google Scholar 

  • Wang KJ, Xing BS (2005) Structural and sorption characteristics of adsorbed humic acid on clay minerals. J Environ Qual 34(1):342–349

    Article  CAS  Google Scholar 

  • Wang S, Dou S, Yu ZG, Ma LN, Li Y, Yu SS (2014) Compositions and properties of microbial residues formed by three single species fungi and mixed strains in cellulose-containing liquid media. J Soil Sci Plant Nutr 14(2):366–381

    CAS  Google Scholar 

  • Wang Q, Yang P, Zhu MQ (2018) Structural transformation of birnessite by fulvic acid under anoxic conditions. Environ Sci Technol 52(4):1844–1853

    Article  CAS  Google Scholar 

  • Wei YQ, Wu D, Wei D, Zhao Y, Wu JQ, Xie XY, Zhang RJ, Wei ZM (2019) Improved lignocellulose-degrading performance during straw composting from diverse sources with actinomycetes inoculation by regulating the key enzyme activities. Bioresour Technol 271:66–74

    Article  CAS  Google Scholar 

  • Wu M, Song MY, Liu M, Jiang CY, Li ZP (2016) Fungicidal activities of soil humic/fulvic acids as related to their chemical structures in greenhouse vegetable fields with cultivation chronosequence. Sci Rep 6(6):32858

    Article  CAS  Google Scholar 

  • Wu JQ, Zhao Y, Qi HS, Zhao XY, Yang TX, Du YQ, Zhang H, Wei ZM (2017a) Identifying the key factors that affect the formation of humic substance during different materials composting. Bioresour Technol 244:1193–1196

    Article  CAS  Google Scholar 

  • Wu JQ, Zhao Y, Zhao W, Yang TX, Zhang X, Xie XY, Cui HY, Wei ZM (2017b) Effect of precursors combined with bacteria communities on the formation of humic substances during different materials composting. Bioresour Technol 226:191–199

    Article  CAS  Google Scholar 

  • Xin Y, Wang JQ, Li YY, Asiri AM, Marwani HM, Hu SH, Wang G, Xu ZM (2018) Influence of humic acid on the immobilization of U(VI) by montmorillonite in simulated environmental conditions. Sep Sci Technol 53(5):696–706

  • Zavarzina AG (2006) A mineral support and biotic catalyst are essential in the formation of highly polymeric soil humic substances. Eurasian Soil Sci+ 39(S1):48–53

    Article  Google Scholar 

  • Zhang LC, Luo L, Zhang SZ (2012) Integrated investigations on the adsorption mechanisms of fulvic and humic acids on three clay minerals. Colloids and Surfaces A: Physicochem Eng Asp 406(20):84–90

    Article  CAS  Google Scholar 

  • Zhang YC, Yue DB, Ma H (2015) Darkening mechanism and kinetics of humification process in catechol-Maillard system. Chemosphere 130:40–45

    Article  CAS  Google Scholar 

  • Zhang ZC, Zhao Y, Wang RX, Lu Q, Wu JQ, Zhang DY, Nie ZF, Wei ZM (2018) Effect of the addition of exogenous precursors on humic substance formation during composting. Waste Manag 79:462–471

    Article  CAS  Google Scholar 

  • Zhao Y, Lu Q, Wei YQ, Cui HY, Zhang X, Wang XQ, Shan S, Wei ZM (2016) Effect of actinobacteria agent inoculation methods on cellulose degradation during composting based on redundancy analysis. Bioresour Technol 219:196–203

    Article  CAS  Google Scholar 

  • Zhao XL, Wang Y, Wu HY, Fang LC, Liang JJ, Fan QH, Li P (2017) Insights into the effect of humic acid on Ni(II) sorption mechanism on illite: Batch, XPS and EXAFS investigations. J Mol Liq 248:1030–1038

  • Zhao G, Li EZ, Li JJ, Xu MY, Huang QY, Rong XM (2018) Effects of interfaces of goethite and humic acid-goethite complex on microbial degradation of methyl parathion. Front Microbiol 9:1748

    Article  Google Scholar 

  • Zhou YL, Zhang YB, Li GH, Wu YD, Jiang T (2015) A further study on adsorption interaction of humic acid on natural magnetite, hematite and quartz in iron ore pelletizing process: Effect of the solution pH value. Powder Technol 271:155–166

    Article  CAS  Google Scholar 

Download references

Funding

This research work was funded by the National Key Research and Development Program of China (funding number 2018YFD0300207-1), the National Natural Science Foundation of China (funding number 41401251), and the Seeded Foundation of Jilin Agricultural Science and Technology University (funding number 20187004).

Author information

Authors and Affiliations

  1. College of Agriculture, Jilin Agricultural Science and Technology University, Jilin, 132101, China

    Shuai Wang, Yu Wang, Jiayan Fan, Lan Liu, Nan Wang & Dianyuan Chen

  2. Department of Biosystems Engineering and Soil Science, Institute of Agriculture, The University of Tennessee, Knoxville, TN, 37996, USA

    Shuai Wang

  3. College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100094, China

    Junping Xu

  4. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Xi Zhang

Authors
  1. Shuai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junping Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiayan Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dianyuan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuai Wang.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(RAR 1975 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, S., Xu, J., Zhang, X. et al. Structural characteristics of humic-like acid from microbial utilization of lignin involving different mineral types . Environ Sci Pollut Res 26, 23923–23936 (2019). https://doi.org/10.1007/s11356-019-05664-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05664-3

Keywords

Search

Navigation