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Journal of Soils and Sediments

, Volume 18, Issue 4, pp 1365–1375 | Cite as

Structure-function relationship of vermicompost humic fractions for use in agriculture

  • Andrés Calderín García
  • Orlando Carlos Huertas Tavares
  • Dariellys Martínez Balmori
  • Vitor dos Santos Almeida
  • Luciano Pasqualoto Canellas
  • José María García-Mina
  • Ricardo Luis Louro Berbara
Natural Organic Matter: Chemistry, Function and Fate in the Environment
First Online:

Abstract

Purpose

The use of humic substances (HS) in agriculture is beneficial and has positive environmental impacts. However, to optimize the use of HS possible links between their structural characteristics and bioactivity must be shown. The goal of this study is to evaluate the bioactivity of different humic fractions extracted from vermicompost (VC) in rice plants and to shed light to possible structure-function relationships.

Materials and methods

Humic-like fractions were obtained from cattle manure vermicompost processed by African nightcrawlers (Eudrilus eugeniae spp.). Humic-like acid fraction using only water as extractor (HLAw), HLA fraction extracted following the International Humic Substances Society (IHSS) recommended method, and the solid residue (humified residual (HR)) after extraction of HLA were characterized using complementary chemical, physic, and spectroscopic technics (elemental composition, UV-Vis and Fourier transform infrared spectroscopy (FTIR) spectroscopies, 13C-CP MAS NMR, and MEV). Biological activity of the three HS was conducted in growth chambers and measured in roots using WinRhizo Arabidopsis software. Principal component analysis (PCA) was used to find a grouping pattern between the structural variables evaluated and the obtained root parameters.

Results and discussion

Differences were found in elemental composition among HS with larger C/N ratio in HR than in HLA and HLAw. HLA and HLAw FTIR spectra showed carboxyl band at 1714.66 cm−1 better resolved than in HR. Bands at 1642 cm−1 (amide I) and 1510 cm−1 (lignin), were better resolved in HLA. 13C-NMR showed the following order of aromaticity: HLA > HLAw > HR. For HLAw bioactivity, the structures CAlkyl-H,R, CC=O, and CCOO-H,R correlated with the number and growth of smaller root. The aromatic CAr-H,R, CAr-O,N, and aliphatic CAlkyl-O,N, CAlkyl-O, and CAlkyl-di-O structures in HLA, correlated with larger roots growth. HR also stimulated root growth and development in rice plants.

Conclusions

Aliphatic and oxygenated structures in HLAw showed a relation with induction of initial root emissions, whereas the presence of aromatic compounds in HLA was related with root growth stimulation activity. Higher concentration of HLAw was necessary to produce an equivalent stimulus compared with HLA; it could indicate that, although both fractions showed similar types of structures in their composition, differences in the predominant structures may be determining different effects on the root.

Keywords

13C NMR spectroscopy Bioactivity Humic substances Vermicompost 
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Notes

Acknowledgments

A.C.G. (sisFaperj 2012028010) thanks FAPERJ for his grant. A.C.G, R.L.L.B, and J.M.G.M thank the CNPq-CAPES for the PDJ scholarship and funding through the project Science without Borders—PVE A060/2013. The authors thank CAPES-MES project no. 46/2013, 215/13.

Supplementary material

11368_2016_1521_MOESM1_ESM.docx (109 kb)
Fig. S1 (DOCX 109 kb)

References

  1. Álvarez MR, Aragonés CR, Padiz AS, Vazquez MM (1998) Lombrices de Tierra con Valor Comercial. Biología y Técnicas de Cultivo [Commercial value of earthworms. Biology and cultivation techniques]. UQROO, Mexico, p 30Google Scholar
  2. Aguiar NO, Novotny EH, Oliveira AL, Rumjanek VM, Olivares FL, Canellas LP (2013) Prediction of humic acids bioactivity using spectroscopy and multivariate analysis. J Geochem Explor 129:95–102CrossRefGoogle Scholar
  3. Amir S, Jouraiphy A, Meddich A, Gharous M, Winterto P, Hafidi M (2010) Structural study of humic acids during composting of activated sludge-green waste: elemental analysis, FTIR and 13C NMR. J Hazard Mater 177:524–529CrossRefGoogle Scholar
  4. Arancon NQ, Edwards CA, Bierman P, Welch C, Metzger JD (2004) Influences of vermicomposts on field strawberries: 1. Effects on growth and yields. Bioresour Technol 932:145–153CrossRefGoogle Scholar
  5. Arancon NQ, Edwards CA, Lee S, Byrne R (2006) Effects of humic acids from vermicomposts on plant growth. Eur J Soil Biol 42:S65–S69CrossRefGoogle Scholar
  6. Atiyeh RM, Subler S, Edwards CA, Bachman G, Metzger JD, Shuster (2000) Effects of vermicomposts and composts on plant growth in horticultural container media and soil. Pedobiologia 44:579–590CrossRefGoogle Scholar
  7. Atiyeh RM, Edwards CA, Subler S, Metzger JD (2001) Pig manure vermicompost as a component of a horticultural bedding plant medium: effects on physicochemical properties and plant growth. Bioresour Technol 78:11–20CrossRefGoogle Scholar
  8. Atiyeh RM, Lee S, Edwards CA, Arancon NQ, Metzger JD (2002) The influence of humic acids derived from earthworm-processed organic wastes on plant growth. Bioresour Technol 84:7–14CrossRefGoogle Scholar
  9. Baigorri R, Fuentes M, González-Gaitano G, García-Mina JM, Almendros G, González-Vila FJ (2009) Complementary multianalytical approach to study the distinctive structural features of the main humic fractions in solution: gray humic acid, brown humic acid, and fulvic acid. J Agri Food Chem 57:3266–3272CrossRefGoogle Scholar
  10. Balmori-Martinez D, Spaccini R, Aguiar NO, Novotny EH, Olivares FL, Canellas L (2014) Molecular characteristics of humic acids isolated from vermicomposts and their relationship to bioactivity. J Agr Food Chem 62:11412–11419CrossRefGoogle Scholar
  11. Berbara RL, García AC (2014) In: Parvaiz A, Mohd RW (eds) Humic substances and plant defense metabolism. Springer, New York, pp. 297–319Google Scholar
  12. Campitelli P, Ceppi S (2008) Effects of composting technologies on the chemical and physicochemical properties of humic acids. Geoderma 144:325–333CrossRefGoogle Scholar
  13. Canellas LP, Olivares FL (2014) Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric 1:1–11CrossRefGoogle Scholar
  14. Canellas LP, Dobbss LB, Oliveira AL, Chagas JG, Aguiar NO, Rumjanek VM, Novotny EH, Olivares FL, Spaccini R, Piccolo A (2012) Chemical properties of humic matter as related to induction of plant lateral roots. Eur J Soil Sci 63:315–324CrossRefGoogle Scholar
  15. Canellas LP, Balmori DM, Médici LO, Aguiar NO, Campostrini E, Rosa RC, Façanha AR, Olivares FL (2013) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366:119–132CrossRefGoogle Scholar
  16. Chai X, Takayuki S, Cao X, Guo Q, Zhao Y (2007) Spectroscopic studies of the progress of humification processes in humic substances extracted from refuse in a landfill. Chemosphere 69:1446–1453CrossRefGoogle Scholar
  17. De la Rosa JM, González-Pérez JA, González-Vila FJ, Knicker H, Araújo MF (2011) Molecular composition of sedimentary humic acids from South West Iberian Peninsula: a multi-proxy approach. Org Geochem 42:791–802CrossRefGoogle Scholar
  18. Doan TT, Ngo PT, Rumpel C, Van Nguyen B, Jouquet P (2013) Interactions between compost, vermicompost and earthworms influence plant growth and yield: a one-year greenhouse experiment. Sci Hortic-Amsterdam 160:148–154CrossRefGoogle Scholar
  19. Droussi Z, D’Orazio V, Hafidi M, Ouatmane A (2009) Elemental and spectroscopic characterization of humic-acid-like compounds during composting of olive mill by-products. J Hazard Mater 163:1289–1297CrossRefGoogle Scholar
  20. García AC, Santos LA, Izquierdo FG, Sperandio MVL, Castro RN, Berbara RLL (2012) Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol Eng 47:203–208CrossRefGoogle Scholar
  21. García AC, Izquierdo FG, Sobrino NMBA, Castro RN, Santos LA, Souza LGA, Berbara RLL (2013) Humified insoluble solid for efficient decontamination of nickel and lead in industrial effluents. J Environ Chem Eng 1:916–924CrossRefGoogle Scholar
  22. García AC, Izquierdo FG, Berbara RLL (2014a) Effects of humic materials on plant metabolism an agricultural productivity. In: P. Ahmad (ed) 1:449–466Google Scholar
  23. García AC, Santos LA, Izquierdo FG, Rumjanek VM, Castro RN, Santos FS, Souza LGA, Berbara RLL (2014b) Potentialities of vermicompost humic acids to alleviate water stress in rice plants (Oryza sativa L.). J Geochem Explor 136:48–54CrossRefGoogle Scholar
  24. García AC, de Souza LGA, Pereira MG, Castro RN, García-Mina JM, Zonta E, Lisboa FJG, Berbara RLL (2016) Structure-property-function relationship in humic substances to explain the biological activity in plants. Sci Rep 6:20798CrossRefGoogle Scholar
  25. González-Pérez JA, González-Vila FJ, Almendros G, Knicker H (2004) The effect of fire on soil organic matter—a review. Environ Int 30:855–870CrossRefGoogle Scholar
  26. Gutiérrez-Miceli FA, Santiago-Borraz J, Molina JAM, Nafate CC, Abud-Archila M, Llaven MAO, Rincón-Rosales R, Dendooven L (2007) Vermicompost as a soil supplement to improve growth, yield and fruit quality of tomato (Lycopersicum esculentum). Bioresour Technol 98:2781–2786CrossRefGoogle Scholar
  27. Hernandez OL, Calderín A, Huelva R, Martínez-Balmori D, Guridi F, Aguiar NO, Olivares FL, Canellas LP (2015) Humic substances from vermicompost enhance urban lettuce production. Agron Sustain Dev 35:225–232CrossRefGoogle Scholar
  28. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Station Bull 347:1–32Google Scholar
  29. IHSS (2013) International Humic Substances Society. Available at: http://www.humicsubstances.org/
  30. Jannin L, Arkoun M, Ourry A, Laîné P, Goux D, Garnica M, Fuentes M, Francisco MM, Baigorri R, Cruz F, Houdusse F, García-Mina JM, Yvin JC, Etienne P (2012) Microarray analysis of humic acid effects on Brassica napus growth: involvement of N, C and S metabolisms. Plant Soil 359:297–319CrossRefGoogle Scholar
  31. Joshi D, Hooda KS, Bhatt JC, Mina BL, Gupta HS (2009) Suppressive effects of composts on soil-borne and foliar diseases of French bean in the field in the western Indian Himalayas. Crop Prot 28:608–615CrossRefGoogle Scholar
  32. Kumar MS, Rajiv P, Rajeshwari S, Venckatesh R (2015) Spectroscopic analysis of vermicompost for determination of nutritional quality. Spectrochim Acta 135:252–255CrossRefGoogle Scholar
  33. Li X, Meiyan X, Jian Y, Zhidong H (2011) Compositional and functional features of humic acid-like fractions from vermicomposting of sewage sludge and cow dung. J Hazard Mater 185:740–748CrossRefGoogle Scholar
  34. Martínez-Balmori D, Olivares FL, Spaccini R, Aguiar KP, Araújo MF, Aguiar NO, Guridi F, Canellas LP (2013) Molecular characteristics of vermicompost and their relationship to preservation of inoculated nitrogen-fixing bacteria. J Anal Appl Pyrol 104:540–550CrossRefGoogle Scholar
  35. Miralles I, Piedra-Buena A, Almendros G, González-Vila FJ, González-Pérez JA (2015) Pyrolytic appraisal of the lignin signature in soil humic acids: assessment of its usefulness as carbon sequestration marker. J Anal Appl Pyrol 113:107–115CrossRefGoogle Scholar
  36. Mora V, Bacaicoa E, Zamarreño AM, Aguirre E, Garnica M, Fuentes M, García-Mina JM (2010) Action of humic acid on promotion of cucumber shoot growth involves nitrate-related changes associated with the root-to-shoot distribution of cytokinins, polyamines and mineral nutrients. J Plant Physiol 167:633–642CrossRefGoogle Scholar
  37. Mora V, Baigorri R, Bacaicoa E, Zamarreno AM, García-Mina JM (2012) The humic acid-induced changes in the root concentration of nitric oxide, IAA and ethylene do not explain the changes in root architecture caused by humic acid in cucumber. Environ Exp Bot 76:24–32CrossRefGoogle Scholar
  38. Muscolo A, Sidari M, Attiná E, Francioso O, Tugnoli V, Nardi S (2007) Biological activity of humic substances is related to their chemical structure. Soil Sci Soc Am J 71:75–85CrossRefGoogle Scholar
  39. Muscolo A, Sidari M, Nardi S (2013) Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J Geochem Explor 129:57–63CrossRefGoogle Scholar
  40. Nebbioso A, Piccolo A (2011) Basis of a humeomics science: chemical fractionation and molecular characterization of humic biosuprastructures. Biomacromolecules 12:1187–1199CrossRefGoogle Scholar
  41. Olivares FL, Aguiar NO, Rosa RCC, Canellas LP (2015) Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes. Sci Hortic-Amsterdam 183:100–108CrossRefGoogle Scholar
  42. Pinton R, Cesco S, De Nobili M, Santi S, Varanini Z (1998) Water- and pyrophosphate-extractable humic substances fractions as a source of iron for Fe-deficient cucumber plants. Biol Fert Soils 26:23–27CrossRefGoogle Scholar
  43. Sahni S, Sarma BK, Singh DP, Singh HB, Singh KP (2008) Vermicompost enhances performance of plant growth-promoting rhizobacteria in Cicer arietinum rhizosphere against Sclerotium rolfsii. Crop Prot 27:369–376CrossRefGoogle Scholar
  44. Salter CE, Edwards CA (2014) The production of Vermicompost Aqueous Solutions or Teas. In: Edwards CA, Arancon NQ, Sherman R (eds) pp 153–164Google Scholar
  45. Santos GA, Camargo FAO (1999) Fundamentos da Matéria Orgânica do Solo: Ecossistemas Tropicais e Subtropicais [Fundamentals of soil organic matter: tropical and subtropical ecosystems]. Ed. Genesis, Porto Alegre, Brasil, p. 102 ppGoogle Scholar
  46. Scaglia B, Nunes RR, Rezende MOO, Tambone F, Adani F (2016) Investigating organic molecules responsible of auxin-like activity of humic acid fraction extracted from vermicompost. Sci Total Environ 562:289–295CrossRefGoogle Scholar
  47. Schmidt W, Santi S, Pinton R, Varanini Z (2007) Water-extractable humic substances alter root development and epidermal cell pattern in Arabidopsis. Plant Soil 300:59–267CrossRefGoogle Scholar
  48. Senesi N, Rizzi FR, Delino P (1996) Fractal dimension of humic acids in aquous suspension as a function of pH and time. Soil Sci Soc Am J 60:1773–1778CrossRefGoogle Scholar
  49. Shirshova LT, Ghabbour EA, Davies G (2006) Spectroscopic characterization of humic acid fractions isolated from soil using different extraction procedures. Geoderma 133:204–216CrossRefGoogle Scholar
  50. Singh R, Sharma RR, Kumar S, Gupta RK, Patil RT (2008) Vermicompost substitution influences growth, physiological disorders, fruit yield and quality of strawberry (Fragaria × ananassa Duch.). Bioresour Technol 99:8507–8511CrossRefGoogle Scholar
  51. Song G, Novotny EH, Simpson AJ, Clapp CE, Hayes MHB (2008) Sequential exhaustive extraction of a Mollisol soil, and characterizations of humic components, including humin, by solid and solution state NMR. Eur J Soil Scie 59:505–516CrossRefGoogle Scholar
  52. Spaccini R, Piccolo A (2007) Molecular characterization of compost at increasing stages of maturity: thermochemolysis-GC-MS and 13C CPMAS-NMR spectroscopy. J Agri Food Chem 55:2303–2311CrossRefGoogle Scholar
  53. Spaccini R, Baiano S, Gigliotti G, Piccolo A (2008) Molecular characterization of a compost and its water-soluble fractions. J Agri Food Chem 56:1017–1024CrossRefGoogle Scholar
  54. Traversa A, Loffredo E, Gattullo CE, Palazzo AJ, Bashore TL, Senesi N (2014) Comparative evaluation of compost humic acids and their effects on the germination of switchgrass (Panicum vigatum L.). J Soils Sediments 14:432–440CrossRefGoogle Scholar
  55. Trevisan S, Botton A, Vaccaro S, Vezzaro A, Quaggiotti S, Nardi S (2011) Humic substances affect Arabidopsis physiology by altering the expression of genes involved in primary metabolism, growth and development. Environ Exp Bot 74:45–55CrossRefGoogle Scholar
  56. Vaccaro S, Muscolo A, Pizzeghello D, Spaccini R, Piccolo A, Nardi S (2009) Effect of a compost and its water-soluble fractions on key enzymes of nitrogen metabolism in maize seedlings. J Agr Food Chem 57:11267–11276CrossRefGoogle Scholar
  57. Zaller JG (2007) Vermicompost as a substitute for peat in potting media: effects on germination, biomass allocation, yields and fruit quality of three tomato varieties. Sci Hortic-Amsterdam 112:191–199CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Andrés Calderín García
    • 1
  • Orlando Carlos Huertas Tavares
    • 1
  • Dariellys Martínez Balmori
    • 2
  • Vitor dos Santos Almeida
    • 3
  • Luciano Pasqualoto Canellas
    • 4
  • José María García-Mina
    • 5
  • Ricardo Luis Louro Berbara
    • 1
  1. 1.Departamento de Solo, Laboratório de Biologia do SoloUniversidade Federal Rural do Rio de Janeiro (UFRRJ)SeropédicaBrazil
  2. 2.Departamento de Química, Instituto de AgronomíaUniversidad Agraria de La Habana (UNAH)San José de las LajasCuba
  3. 3.Instituto de QuímicaUniversidade Federal Rural do Rio de Janeiro (UFRRJ)SeropédicaBrazil
  4. 4.Núcleo de Desenvolvimento de Insumos Biológicos para a Agricultura (NUDIBA)Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF)RJBrazil
  5. 5.Department of Environmental Biology, Agricultural Chemistry and Biology Group—CMI Roullier, Faculty of SciencesUniversity of NavarraPamplonaSpain

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