The Soil Humeome: Chemical Structure, Functions and Technological Perspectives

  • Alessandro PiccoloEmail author
  • Riccardo Spaccini
  • Davide Savy
  • Marios Drosos
  • Vincenza Cozzolino


Humus or humic substances (HS) are of pivotal importance in the global ecosystem dynamics, since fluctuation in their amount affects not only the growth of both plants and soil microorganisms, but also the main biogeochemical cycles. The development of technologies aimed at controlling HS in the agroecosystem processes is hindered by the limited knowledge of their chemical structure and dynamics. The recent acknowledgement of the supramolecular nature of soil HS allowed to devise a fractionation procedure, called Humeomics, that enables a detailed characterization of the structure of humic molecules in soil. Humeomics produces homogeneous fractions by progressively breaking esters and ether C–O bonds but not carbon–carbon bonds. The molecules in fractions are then identified by means of advanced spectroscopic and mass spectrometric techniques, thereby providing a body of structures that may well represent the soil Humeome. Humeomics enabled to unravel the effects of different soil management practices on soil carbon dynamics and to explain the recalcitrance of HS in soil. Moreover, the application of Humeomics allowed to corroborate the novel concept of humification, that is unambiguously described as the progressive accumulation of hydrophobic molecular components, which are no longer biotically accessible, due to their rapid thermodynamically driven partitioning from liquid to the solid soil phases. Conceiving HS as supramolecular associations of relatively small compounds also helped to unravel the reactivity of HS with respect to plant and microbial development, as well as towards xenobiotics. Finally, the supramolecular understanding of HS encouraged the proposal of an innovative technology for the control of organic matter stabilization in soil. This is based on the in situ photo-polymerization of humic molecules catalysed by metal porphyrin biomimetic catalysts. The resulting increase in the molecular mass of humic molecules was found not only to increase soil aggregate stability but also to sequester in soil significant yearly amounts of organic carbon. It is expected that the research findings presented here will prompt novel studies on the man-driven control of the soil Humeome in order to increase its content in soil, and contribute to positively affect both crop yields and soil microbial activity.


Humus supramolecular structure Soil Humeome Humeomics Humification Recalcitrance of soil carbon Carbon sequestration 


  1. Achard FK (1786). Chemische untersuchung des torfs. Crell’s Chem Ann 2:391–403Google 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 Expl 129:95–102Google Scholar
  3. Aguiar NO, Medici LO, Olivares FL, Dobbss LB, Torres-Netto A, Silva SF, Novotny EH, Canellas LP (2016) Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann Appl Biol 168(203–213):2016Google Scholar
  4. Aguirre E, Leménager D, Bacaicoa E, Fuentes M, Baigorri R, Zamarreño AM, García-Mina JM (2009) The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol Biochem 47:215–223PubMedGoogle Scholar
  5. Baalousha M, Motelica-Heino M, Galaup S, Le Coustumer P (2005) Supramolecular structure of humic acids by TEM with improved sample preparation and staining. Microsc Res Technol 66:299–306Google Scholar
  6. Baalousha M, Motelica-Heino M, Le Coustumer P (2006) Conformation and size of humic substances: effects of major cation concentration and type, pH, salinity and residence time. Colloids Surf A 272:48–55Google Scholar
  7. Baldock JA, Skjiemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31:697–710Google Scholar
  8. Buurman P, van Lagen B, Piccolo A (2002) Increase in stability against thermal oxidation of soil humic substances as a result of self- association. Org Geochem 33:367–381Google Scholar
  9. Canellas LP, Olivares FL (2014) Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric 1:3Google Scholar
  10. Canellas LP, Olivares FL (2017) Production of border cells and colonization of maize root tips by Herbaspirillum seropedicae are modulated by humic acid. Plant Soil 417:403–413Google Scholar
  11. Canellas LP, Teixeira Junior LRL, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Façanha AR (2008) Humic acids cross-interactions with root and organic acids. Ann Appl Biol 153:157–166Google Scholar
  12. Canellas LP, Dantas DJ, Aguiar NO, Peres LEP, Zsögön A, Olivares FL, Dobbss LB, Façanha AR, Nebbioso A, Piccolo A (2011) Probing the hormonal activity of fractionated molecular humic components in tomato auxin mutants. Ann Appl Biol 159:202–211Google Scholar
  13. 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 63:315–324Google Scholar
  14. Canellas LP, Olivares FL, Aguiar N, Jones DL, Nebbioso A, Mazzei P, Piccolo A (2015) Humic and fulvic acids as biostimulants in horticulture. Sci Hortic 196:15–27Google Scholar
  15. Chen Y (1996) Organic matter reactions involving micronutrients in soils and their effect on plants. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 507–530Google Scholar
  16. Chilom G, Bruns AS, Rice JA (2009) Aggregation of humic acids in solution: contribution of different fractions. Org Geochem 40:455–460Google Scholar
  17. Conte P, Piccolo A (1999) Conformational arrangement of dissolved humic substances. Influence of solution composition on association of humic molecules. Environ Sci Technol 33:1682–1690Google Scholar
  18. Conte P, Zena A, Pilidis G, Piccolo A (2001) Increased retention of Polyaromatic Hydrocarbons (PAH) in soils induced by soil treatment with humic substances. Environ Pollut 112:27–31Google Scholar
  19. Conte P, Spaccini R, Piccolo A (2006) Advanced CPMAS-13C NMR techniques for molecular characterization of size-separated fractions from a soil humic acid. Anal Bioanal Chem 386:382–390PubMedGoogle Scholar
  20. Conte P, Spaccini R, Šmejkalová D, Nebbioso A, Piccolo A (2007) Spectroscopic and conformational properties of size-fractions separated from a lignite humic acid. Chemosphere 69:1032–1039PubMedGoogle Scholar
  21. Cozzolino A, Piccolo A (2002) Polymerization of dissolved humic substances catalyzed by peroxidase. Effects of pH and humic composition. Org Geochem 33:281–294Google Scholar
  22. Cozzolino A, Conte P, Piccolo A (2001) Conformational changes of humic substances induced by some hydroxy-, keto-, and sulfonic acids. Soil Biol Bochem 33:563–571Google Scholar
  23. Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44Google Scholar
  24. Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo A (2016a) The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fertil Soils 52:15–29Google Scholar
  25. Cozzolino V, De Martino A, Di Meo V, Salluzzo A, Piccolo A (2016b) Plant tolerance to mercury in a contaminated soil is enhanced by the combined effects of humic matter addition and inoculation with arbuscular mycorrhizal fungi. Environ Sci Pollut Res 23:11312–11322Google Scholar
  26. da Piedade Melo A, Olivares FL, Médici LO, Dobbss LB, Torres-Netto A, Canellas LP (2017) Mixed rhizobia and Herbaspirillum seropedicae inoculations with humic acid-like substances improve water-stress recovery in common beans. Chem Biol Technol Agric 4:6. Scholar
  27. Dobbss LB, Canellas PL, Lopes Olivares F, Aguiar ON, Peres LEP, Azevedo M, Spaccini R, Piccolo A, Façanha AR (2010) Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J Agric Food Chem 58:3681–3688PubMedGoogle Scholar
  28. Drosos M, Piccolo A (2018) The molecular dynamics of soil humus as a function of tillage. Land Degr Develop 29:1792–1805. Scholar
  29. Drosos M, Nebbioso A, Mazzei P, Vinci G, Spaccini R, Piccolo A (2017) A molecular zoom into soil Humeome by a direct sequential chemical fractionation of soil. Sci Total Environ 15:807–816Google Scholar
  30. Drosos M, Nebbioso A, Piccolo A (2018a) Humeomics: a key to unravel the humusic pentagram. Appl Soil Ecol 123:513–516Google Scholar
  31. Drosos M, Savy D, Spiteller M, Piccolo A (2018b) Structural characterization of carbon and nitrogen molecules in the Humeome of two different grassland soils. Chem Biol Technol Agric 5:14Google Scholar
  32. Fava F, Piccolo A (2002) Effects of humic substances on the bioavailability and aerobic biodegradation of polychlorinated biphenyls in a model soil. Biotechnol. Bioeng 77(2):204–211Google Scholar
  33. Feng XJ, Simpson AJ, Simpson MJ (2005) Chemical and mineralogical controls on humic acid sorption to clay mineral surfaces. Org Geochem 36:1553–1566Google Scholar
  34. Fiorentino G, Spaccini R, Piccolo A (2006) Separation of molecular constituents from a humic acid by solid-phase extraction following a transesterification reaction. Talanta 68:1135–1142PubMedGoogle Scholar
  35. García AC, Santos LA, Ambrósio de Souza LG, Tavares OCH, Zonta E, Gomes ETM, García-Mina JM, Berbara RLL (2016) Vermicompost humic acids modulate the accumulation and metabolism of ROS in rice plants. J Plant Physiol 192:56–63PubMedGoogle Scholar
  36. Gelsomino A, Tortorella D, Cianci V, Petrovicová B, Sorgonà A, Piccolo A et al (2010) Effects of a biomimetic iron-porphyrin on soil respiration and maize root morphology as by a microcosm experiment. J Plant Nutr Soil Sci 173:399–406Google Scholar
  37. Grignani C, Alluvione F, Bertora C, Zavattaro L, Fagano M, Fiorentino N, et al (2012) Field plots and crop yields under innovative methods of carbon sequestration in soil. In: Piccolo A (ed) Carbon sequestration in agricultural soils: a multidisciplinary approach to innovative methods. Springer, Heidelberg, Berlin, pp 39–60Google Scholar
  38. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52:265–275PubMedGoogle Scholar
  39. Hayes MHB (2009) Evolution of concepts of environmental natural nonliving organic matter. In: Senesi N, Xing B, Huang PM (eds) Biophysico-chemical processes involving natural nonliving organic matter in environmental systems. Wiley, New Jersey, pp 1–39Google Scholar
  40. Hertkorn N, Benner R, Frommberger M, Schmitt-Kopplin P, Witt M, Kaiser K et al (2006) Characterization of a major refractory component of marine dissolved organic matter. Geochim Cosmochim Acta 70:2990–3010Google Scholar
  41. Incerti G, Bonanomi G, Giannino F, Carteni F, Spaccini R, Mazzei P et al (2017) OMDY: a new model of organic matter decomposition based on biomolecular contentas assessed by 13C-CPMAS-NMR. Plant Soil 411:377–394Google Scholar
  42. Insam H (1996) Microorganisms and humus in soils. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, The Netherlands, pp 361–406Google Scholar
  43. Jindo K, Soares TS, Peres LEP, Azevedo IG, Aguiar NO, Mazzei P, Spaccini R, Piccolo A, Olivares FL, Canellas LP (2016) Phosphorus speciation and high-affinity transporters are influenced by humic substances. J Plant Nutr Soil Sci 179:206–214Google Scholar
  44. Kelley KR, Stevenson FJ (1996) Organic forms of N in soil. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, The Netherlands, pp 407–427Google Scholar
  45. Kleber M, Sollins P, Sutton R (2007) A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85:9–24Google Scholar
  46. Köchy M, Hiederer R, Freibauer A (2015) Global distribution of soil organic carbon—Part 1: masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wet-lands, and the world. Soil 1:351–365Google Scholar
  47. Kozak J (1996) Soil organic matter as a factor influencing the fate of organic chemicals in the soil environment. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, The Netherlands, pp 652–664Google Scholar
  48. Li M, Cozzolino V, Mazzei P, Drosos M, Monda H, Hu Z, Piccolo A (2017) Effects of microbial bioeffectors and P amendments on P forms in a maize cropped soil as evaluated by 31P–NMR spectroscopy. Plant Soil 427:87–104. Scholar
  49. Lipczynska-Kochany E (2018) Humic substances, their microbial interactions and effects on biological transformations of organic pollutants in water and soil: a review. Chemosphere 202:420–437PubMedGoogle Scholar
  50. Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 142:1–10Google Scholar
  51. Lovley DR, Coates JD, Blunt-Harris EL, Phillips JP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 282:445–448Google Scholar
  52. Magid J, Tiessen H, Condron LM (1996) Dynamics of organic phosphorus in soils under natural and agricultural ecosystems. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, The Netherlands, pp 429–466Google Scholar
  53. Maia CM, Piccolo A, Mangrich AS (2008) Molecular size distribution of compost-derived humates as a function of concentration and different counterions. Chemosphere 73:1162–1166PubMedGoogle Scholar
  54. Mao J, Fang X, Schmidt-Rohr K, Carmo AM, Hundal LS, Thompson M-L (2007) Molecular-scale heterogeneity of humic acid in particle-size fractions of two Iowa soils. Geoderma 140:17–29Google Scholar
  55. Martinez-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 Pyr 104:540–550Google Scholar
  56. Martinez-Balmori D, Spaccini R, Aguiar NO, Novotny EH, Olivares FL, Canellas LP (2014) Molecular characteristics of humic acids isolated from vermicomposts and their relationship to bioactivity. J Agric Food Chem 62:11412–11419PubMedGoogle Scholar
  57. Masoom H, Courtier-Murias D, Farooq H, Soong R, Kelleher BP, Zhang C et al (2016) Soil organic matter in its native state: unravelling the most complex biomaterial on earth. Environ Sci Technol 50:1670–1680PubMedGoogle Scholar
  58. Mazzei P, Piccolo A (2012) Quantitative evaluation of noncovalent interactions between glyphosate and dissolved humic substances by NMR spectroscopy. Environ Sci Technol 46:5939–5946PubMedGoogle Scholar
  59. Mazzoleni S, Bonanomi G, Giannino F, Incerti G, Piermatteo D, Spaccini R et al (2012) New modeling approach to describe and predict carbon sequestration dynamics in agricultural soils. In: Piccolo A (ed) Carbon sequestration in agricultural soils. Springer, Berlin, pp 291–307Google Scholar
  60. Minasny B, Malone BP, McBratney AB, Angers DA, Arrouays D, Chambers A, Chaplot V, Chen Z-S, Cheng K, Das BS, Field DJ, Gimona A, Hedley CB, Hong SY, Mandal B, Marchant BP, Martin M, McConkey BG, Mulder VL, O’Rourke S, Richer-de-Forges AC, Odeh I, Padarian J, Paustian K, Pan G, Poggio L, Savin I, Stolbovoy V, Stockmann U, Sulaeman Y, Tsui C-C, Vågen T-G, van Wesemael B, Winowiecki L (2017) Soil carbon 4 per mille. Geoderma 292:59–86. Scholar
  61. Monda H, Cozzolino V, Vinci G, Spaccini R, Piccolo A (2017) Molecular characteristics of water-extractable organic matter from different composted biomasses and their effects on seed germination and early growth of maize. Sci Total Environ 590–591:40–49PubMedGoogle Scholar
  62. Monda H, Cozzolino V, Vinci G, Drosos M, Savy D, Piccolo A (2018) Molecular composition of the Humeome extracted from different green composts and their biostimulation on early growth of maize. Plant Soil 429:407–424Google Scholar
  63. Mora V, Bacaicoa E, Zamarreño AM, Aguirre E, Garnica M, Fuentes M, Garcia-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 167:633–642PubMedGoogle Scholar
  64. Muscolo A, Sidari M, Nardi R (2013) Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J Geochem Explor 129:57–63Google Scholar
  65. Nardi S, Muscolo A, Vaccaro S, Baiano S, Spaccini R, Piccolo A (2007) Relationship between molecular characteristics of soil humic fractions and glycolytic pathway and krebs cycle in maize seedlings. Soil Biol Biochem 39:3138–3146Google Scholar
  66. Nardi S, Ertani A, Francioso O (2017) Soil–root cross-talking: the role of humic substances. J Plant Nutr Soil Sci 180:5–13Google Scholar
  67. Nebbioso A, Piccolo A (2009) Molecular rigidity and diffusivity of Al3+ and Ca2+ humates as revealed by NMR spectroscopy. Environ Sci Technol 43:2417–2424PubMedGoogle Scholar
  68. Nebbioso A, Piccolo A (2011) Basis of a humeomics science: chemical fractionation and molecular characterization of humic biosuprastructures. Biomacromol 12:1187–1199Google Scholar
  69. Nebbioso A, Piccolo A (2012) Advances in humeomics: enhanced structural identification of humic molecules after size fractionation of a soil humic acid. Anal Chim Acta 720:77–90PubMedGoogle Scholar
  70. Nebbioso A, Piccolo A (2013) Molecular characterization of dissolved organic matter (DOM): a critical review. Anal Bioanal Chem 405:109–124PubMedGoogle Scholar
  71. Nebbioso A, Piccolo A, Spiteller M (2010) Limitations of electrospray ionization in the analysis of a heterogeneous mixture of naturally occurring hydrophilic and hydrophobic compounds. Rapid Commun Mass Spectrom 24:3163–3170PubMedGoogle Scholar
  72. Nebbioso A, Piccolo A, Lamshöft M, Spiteller M (2014a) Molecular characterization of an end-residue of humeomics applied to a soil humic acid. RSC Adv. 4:23658–23665Google Scholar
  73. Nebbioso A, Mazzei P, Savy D (2014b) Reduced complexity of multidimensional and diffusion NMR spectra of soil humic fractions as simplified by humeomics. Chem Biol Technol Agric 1:24. Scholar
  74. Nebbioso A, Vinci G, Drosos M, Spaccini R, Piccolo A (2015) Unveiling the molecular composition of the unextractable soil organic fraction (humin) by humeomics. Biol Fertil Soils 51:443–451Google Scholar
  75. Nuzzo A, Piccolo A (2013) Oxidative and photo-oxidative polymerization of humic suprastructures by heterogeneous biomimetic catalysis. Biomacromolecules 14:1645–1652PubMedGoogle Scholar
  76. Nuzzo A, Sánchez A, Fontaine B, Piccolo A (2013) Conformational changes of dissolved humic and fulvic superstructures with progressive iron complexation. J Geochem Explor 129:1–5Google Scholar
  77. Nuzzo A, Madonna E, Mazzei P, Spaccini R, Piccolo A (2016) In situ photo-polymerization of soil organic matter by heterogeneous nano-TiO2 and biomimetic metal-porphyrin catalysts. Biol Fertil Soils 52:585–593Google Scholar
  78. Nuzzo A, Spaccini R, Cozzolino V, Moschetti G, Piccolo A (2017) In situ polymerization of soil organic matter by oxidative biomimetic catalysis. Chem Biol Technol Agric 4:12Google Scholar
  79. Nuzzo A, De Martino A, Di Meo V, Piccolo A (2018) Potential alteration of iron–humate complexes by plant root exudates and microbial siderophores. Chem Biol Technol Agric 5:19. Scholar
  80. Oades JM (1988) The retention of organic matter in soils. Biogeochemistry 5:35–70Google Scholar
  81. Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:825–828Google Scholar
  82. Olaetxea M, Mora V, Bacaicoa E, Garnica M, Fuentes M, Casanova E, Zamarreño AM, Iriarte JC, Etayo D, Ederra I, Gonzalo R, Baigorri R, Gonzalo R, Garcia-Mina J-M (2015) Abscisic acid regulation of root hydraulic conductivity and aquaporin gene expression is crucial to the plant shoot growth enhancement caused by rhizosphere humic acids. Plant Physiol 169:2587–2596Google Scholar
  83. Olaetxea M De, Hita D, Garcia A, Fuentes M, Baigorri R, Mora V, Garnica M, Urrutia O, Zamarreño AM, Berbara RL, Garcia-Mina JM (2018) Hypothetical framework integrating the main mechanisms involved in the promoting action of rhizospheric humic substances on plant root- and shoot-growth. Appl Soil Ecol 123:521–537Google Scholar
  84. Orlowska E, Roller A, Pignitter M, Jirsa F, Krachler R, Kandioller W, Keppler BK (2017) Synthetic iron complexes as models for natural iron-humic compounds: synthesis, characterization and algal growth experiments. Sci Tot Environ 577:94–104Google Scholar
  85. Orsi M (2014) Molecular dynamics simulation of humic substances. Chem Biol Technol Agric 1:10. Scholar
  86. Pane C, Spaccini R, Piccolo A, Scala F, Bonanomi G (2011) Compost amendments enhance peat suppressiveness to Pythium ultimum, Rhizoctonia solani and Sclerotinia minor. Biol Control 56:115–124Google Scholar
  87. Pane C, Piccolo A, Spaccini R, Celano G, Villecco D, Zaccardelli M (2013) Agricultural waste-based composts exhibiting suppressivity to diseases caused by the phytopathogenic soil-borne fungi Rhizoctonia solani and Sclerotinia minor. Appl Soil Ecol 65:43–51Google Scholar
  88. Pane P, Celano G, Piccolo A, Villecco D, Spaccini R, Palese AM, Zaccardelli M (2015) Effects of on-farm composted tomato residues on soil biological activity and yields in a tomato cropping system. Chem Biol Technol Agric 2:4. Scholar
  89. Paul EA (2016) The nature and dynamics of soil organic matter: Plant inputs, microbial transformations, and organic matter stabilization. Soil Biol Biochem 98:109–126Google Scholar
  90. Peuravuori J (2005) NMR spectroscopy study of freshwater humic material in light of supramolecular assembly. Environ Sci Technol 39:5541–5549PubMedGoogle Scholar
  91. Peuravuori J, Pihlaja K (2004) Preliminary study of lake dissolved organic matter in light of nanoscale supramolecular assembly. Environ Sci Technol 38:5958–5967PubMedGoogle Scholar
  92. Peuravuori J, Bursakova P, Pihlaja K (2007) ESI-MS analyses of dissolved organic matter in light of supramolecular assembly. Anal Bioanal Chem 389:1559–1568PubMedGoogle Scholar
  93. Piccolo A (1996) Humus and soil conservation. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, The Netherlands, pp 225–264Google Scholar
  94. Piccolo A (1989) Reactivity of humic substances towards plant available heavy metals. Sci Total Environ 81/82:607–614Google Scholar
  95. Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166:810–832Google Scholar
  96. Piccolo A (2002) The supramolecular structure of humic substances: a novel understanding of humus chemistry and implications in soil science. Adv Agr 75:57–134Google Scholar
  97. Piccolo A (2012) The nature of soil organic matter and innovative soil managements to fight global changes and maintain agricultural productivity. In: Piccolo A (ed) Carbon sequestration in agricultural soils. Springer, Heidelberg, pp 1–19Google Scholar
  98. Piccolo A (2016) In memoriam Prof. F. J. Stevenson and the question of humic substances in soil. Chem Biol Technol Agric 3:23.
  99. Piccolo A, Mbagwu JSC (1999) Role of hydrophobic components of soil organic matter in soil aggregate stability. Soil Sci Soc Am J 63:1801–1810Google Scholar
  100. Piccolo A, Spiteller M (2003) Electrospray ionization mass spectrometry of terrestrial humic substances and their size-fractions. Anal Bioanal Chem 377:1047–1059PubMedGoogle Scholar
  101. Piccolo A, Nardi S, Concheri G (1992) Structural characteristics of humic substances as related to nitrate uptake and growth regulation in plant systems. Soil Biol Biochem 24:373–380Google Scholar
  102. Piccolo A, Nardi S, Concheri G (1996) Macromolecular changes of soil humic substances induced by interactions with organic acids. Eur J Soil Sci 47:319–328Google Scholar
  103. Piccolo A, Cozzolino A, Conte P, Spaccini R (2000) Polymerization of humic substances by an enzyme-catalyzed oxidative coupling. Naturwissenschaften 87:391–394PubMedGoogle Scholar
  104. Piccolo A, Conte P, Cozzolino A (2001) Chromatographic and spectrophotometric properties of dissolved humic substances compared with macromolecular polymers. Soil Sci 166:174–185Google Scholar
  105. Piccolo A, Conte P, Spaccini R, Chiarella M (2003) Effects of some dicarboxylic acids on the association of dissolved humic substances. Biol Fertil Soils 37:255–259Google Scholar
  106. Piccolo A, Spaccini R, Nieder R, Richter J (2004) Sequestration of a biologically labile organic carbon in soils by humified organic matter. Clim Change 67:329–343Google Scholar
  107. Piccolo A, Conte P, Spaccini R, Mbagwu JSC (2005a) Influence of land use on the humic substances of some tropical soils of Nigeria. Eur J Soil Sci 56:343–352Google Scholar
  108. Piccolo A, Conte P, Tagliatesta P (2005b) Increased conformational rigidity of humic substances by oxidative biomimetic catalysis. Biomacromol 6:351–358Google Scholar
  109. Piccolo A, Spiteller M, Nebbioso A (2010) Effects of sample properties and mass spectroscopic parameters on electrospray ionization mass spectra of size-fractions from a soil humic acid. Anal Bioanal Chem 397:3071–3078PubMedGoogle Scholar
  110. Piccolo A, Spaccini R, Nebbioso A, Mazzei P (2011) Carbon sequestration in soil by in situ catalyzed photo-oxidative polymerization of soil organic matter. Environ Sci Technol 45:6697–6702PubMedGoogle Scholar
  111. Piccolo A, Spaccini R, Drosos M, Cozzolino V (2018a) The molecular composition of humus carbon: recalcitrance and reactivity in soils. In: Garcia C, Nannipieri P, Hernandez T (eds) The future of soil carbon-its conservation and formation. Academic Press, San Diego, pp 87–124Google Scholar
  112. Piccolo A, Spaccini R, Cozzolino V, Nuzzo A, Drosos M, Zavattaro L, Grignani C, Puglisi E, Trevisan M (2018b) Effective carbon sequestration in Italian agricultural soils by in situ polymerization of soil organic matter under biomimetic photocatalysis. Land Degrad Develop 29:485–494. Scholar
  113. Puglisi E, Trevisan M (2012) Effects of methods of carbon sequestration in soil on biochemical indicators of soil quality. In: Piccolo A (ed) Carbon sequestration in agricultural soils. Springer, Heidelberg, pp 179–207Google Scholar
  114. Puglisi E, Fragoulis G, Ricciuti P, Cappa F, Spaccini R, Piccolo A, Trevisan M, Crecchio C (2009) Effects of a humic acid and its size-fractions on the bacterial community of soil rhizosphere under maize (Zea mays L.). Chemosphere 77:829–837PubMedGoogle Scholar
  115. Puglisi E, Pascazio S, Suciu N, Cattani I, Fait G, Spaccini R, Crecchio C, Piccolo A, Trevisan M (2013) Rhizosphere microbial diversity as influenced by humic substance amendments and chemical composition of rhizodeposits. J Geochem Explor 129:82–94Google Scholar
  116. Ramos AC, Olivares FL, Silva LS, Aguiar NO, Canellas LP (2015) Humic matter elicits proton and calcium fluxes and signaling dependent on Ca2+-dependent protein kinase (CDPK) at early stages of lateral plant root development. Chem Biol Technol Agric 2:4. Scholar
  117. Rose MT, Patti AF, Little KR, Brown AL, Jackson WR, Cavagnaro TR (2014) A meta-analysis and review of plant-growth response to humic substances: practical implications for agriculture. Adv Agron 124:37–89Google Scholar
  118. Saiz-Jimenez J (1995) Reactivity of the aliphatic humic moiety in analytical pyrolysis. Org Geochem 23:955–961Google Scholar
  119. Sannino F, Piccolo A (2013) Effective remediation of contaminated soils by eco-compatible chemical, biological and biomimetic practices. In: Basile A, Piemonte V, de Falco M (eds) Sustainable development in chemical engineering: innovative technologies. Wiley, Chichester (UK), pp 267–296Google Scholar
  120. Sarker TC, Incerti G, Spaccini R, Piccolo A, Mazzoleni S, Bonanomi G (2018) Linking organic matter chemistry with soil aggregate stability: Insight from 13C NMR spectroscopy. Soil Biol Biochem 117:175–184Google Scholar
  121. Savy D, Piccolo A (2014) Physical-chemical characteristics of lignins separated from biomasses for second-generation ethanol. Biomass Bioenergy 62:58–67Google Scholar
  122. Savy D, Cozzolino V, Vinci G, Nebbioso A, Piccolo A (2015) Water-soluble lignins from different bioenergy crops stimulate the early development of maize (Zea mays, L.). Molecules 20:19958–19970PubMedPubMedCentralGoogle Scholar
  123. Savy D, Cozzolino V, Nebbioso A, Drosos M, Nuzzo A, Mazzei P, Piccolo A (2016a) Humic-like bioactivity on emergence and early growth of maize (Zea mays L.) of water-soluble lignins isolated from biomass for energy. Plant Soil 402:221–233Google Scholar
  124. Savy D, Mazzei P, Nebbioso A, Drosos M, Nuzzo A, Cozzolino V, Spaccini R, Piccolo A (2016b) Molecular properties and functions of humic substances and humic-like substances (hulis) from biomass and their transformation products. In: Vaz S Jr (ed) Analytical techniques and methods for biomass. Springer, Chan, pp 85–114Google Scholar
  125. Savy D, Mazzei P, Drosos M, Cozzolino V, Lama L, Piccolo A (2017) Molecular characterization of extracts from biorefinery wastes and evaluation of their plant biostimulation. ACS Sustain Chem Eng 5:9023–9031Google Scholar
  126. Savy D, Cozzolino V, Drosos M, Mazzei P, Piccolo A (2018) Replacing calcium with ammonium counterion in lignosulfonates from paper mills affects their molecular properties and bioactivity. Sci Total Environ 645:411–418PubMedGoogle Scholar
  127. 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 562:289–295PubMedGoogle Scholar
  128. Schaumann GE, Thiele-Bruhn S (2011) Reprint of: molecular modeling of soil organic matter: squaring the circle? Geoderma 169:55–68Google Scholar
  129. Schwarzenbach RP, Gschwend PM, Imboden DM (2003a) Sorption III: sorption processes involving inorganic surfaces. In: Environmental organic chemistry, 2nd edn. Wiley Interscience, pp 387–458Google Scholar
  130. Schwarzenbach RP, Gschwend PM, Imboden DM (2003b) Sorption I: general introduction and sorption processes involving organic matter. In: Environmental organic chemistry, 2nd edn. Wiley Interscience, pp 275–330Google Scholar
  131. Scotti R, Pane P, Spaccini R, Palese AM, Piccolo A, Celano G et al (2016) On-farm compost: a useful tool to improve soil quality under intensive farming systems. Appl Soil Ecol 107:13–23Google Scholar
  132. Siéliéchi JM, Lartiges BS, Kayem GJ et al (2008) Changes in humic acid conformation during coagulation with ferric chloride: implications for drinking water treatment. Water Res 42:2111–2123PubMedGoogle Scholar
  133. Simpson AJ (2002) Determining the molecular weight, aggregation, structures and interactions of natural organic matter using diffusion ordered spectroscopy. Magn Reson Chem 40:S72–S82Google Scholar
  134. Six J, Bossuyt H, Degryze S, Denef K (2004) A hystory of research on the link between microaggregates, soil biota and soil organic matter dynamics. Soil Till Res 79:7–31Google Scholar
  135. Šmejkalová D, Piccolo A (2006) Rates of oxidative coupling of humic phenolic monomers catalyzed by a biomimetic iron-porphyrin. Environ Sci Technol 40:1644–1649PubMedGoogle Scholar
  136. Šmejkalová D, Piccolo A (2008a) Aggregation and disaggregation of humic supramolecular assemblies by NMR diffusion ordered spectroscopy (DOSY-NMR). Environ Sci Technol 42:699–706PubMedGoogle Scholar
  137. Šmejkalová D, Piccolo A (2008b) Host-guest interactions between 2,4-dichlorophenol and humic substances as evaluated by 1H NMR relaxation and diffusion ordered spectroscopy. Environ Sci Technol 42:8440–8445PubMedGoogle Scholar
  138. Šmejkalová D, Piccolo A, Spiteller M (2006) Oligomerization of humic phenolic monomers by oxidative coupling under biomimetic catalysis. Environ Sci Technol 40:6955–6962PubMedGoogle Scholar
  139. Šmejkalová D, Spaccini R, Fontaine B, Piccolo A (2009) Binding of phenol and differently halogenated phenols to dissolved humic matter as measured by NMR spectroscopy. Environ Sci Technol 43:5377–5382PubMedGoogle Scholar
  140. Smith PM, Bustamante H, Ahammad H, Clark H, Dong EA, Elsiddig H, et al (2014) Agriculture, forestry and other land use (AFOLU). In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Climate change 2014: mitigation of climate change. Contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cam-bridge, United Kingdom and New York, NY, United States, pp. 816–887. Environ Pollut 241:265–271Google Scholar
  141. Song XY, Spaccini R, Piccolo A, Pan GX (2013) Stabilization by hydrophobic protection as a molecular mechanism for organic carbon sequestration in maize amended rice paddy soils. Sci Total Environ 458:319–330PubMedGoogle Scholar
  142. Spaccini R, Piccolo A (2007) Molecular characterization of compost at increasing stages of maturity. 2. thermochemolysis-GC–MS and 13C-CPMAS-NMR spectroscopy. J Agric Food Chem 55:2303–2311PubMedGoogle Scholar
  143. Spaccini R, Piccolo A (2009) Molecular characteristics of humic acids extracted from compost at increasing maturity stages. Soil Biol Biochem 41:1164–1172Google Scholar
  144. Spaccini R, Piccolo A (2012) Carbon sequestration in soils by hydrophobic protection and in-situ catalyzed photo-polymerization of soil organic matter (SOM). Chemical and physical-chemical aspects of SOM in field plots. In: Piccolo A (ed) Carbon sequestration in agricultural soils. Springer, Heidelberg, pp 61–105Google Scholar
  145. Spaccini R, Piccolo A, Haberhauer G, Gerzabek M (2000) Transformation of organic matter from maize residues into labile and humic fractions of three European soils as revealed by 13C distribution and CPMAS-NMR spectra. Eur J Soil Sci 51:583–594Google Scholar
  146. Spaccini R, Piccolo A, Mbagwu JSC, Igwe CA, Zena TA (2002a) Influence of the addition of organic residues on carbohydrate content and structural stability of some highland soils in Ethiopia. Soil Use Manag 18:404–411Google Scholar
  147. Spaccini R, Piccolo A, Conte P, Haberhauer G, Gerzabek MH (2002b) Increased soil organic carbon sequestration through hydrophobic protection by humic substances. Soil Biol Biochem 34:1839–1851Google Scholar
  148. Spaccini R, Mbagwu JSC, Igwe CA, Conte P, Piccolo A (2004) Carbohydrates and aggregation in lowland soils of Nigeria as influenced by organic inputs. Soil Tillage Res 75:161–172Google Scholar
  149. Spaccini R, Mbagwu JSC, Conte P, Piccolo A (2006) Changes of humic substances characteristics from forested to cultivated soils in Ethiopia. Geoderma 132:9–19Google Scholar
  150. Spaccini R, Sannino D, Piccolo A, Fagnano M (2009) Molecular changes in organic matter of a compost-amended soil. Eur J Soil Sci 60:287–296Google Scholar
  151. Spaccini R, Song X-Y, Cozzolino V, Piccolo A (2013) Molecular evaluation of soil organic matter characteristics in three agricultural soils by improved off-line thermochemolysis: the effect of hydrofluoric acid demineralization treatment. Anal Chim Acta 802:46–55PubMedGoogle Scholar
  152. Spaccini R, Cozzolino V, Di Meo V, Savy D, Drosos M, Piccolo A (2019) Bioactivity of humic substances and water extracts from compost made by ligno-cellulose wastes from biorefinery. Sci Total Environ 646:792–800PubMedGoogle Scholar
  153. Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd ed, Wiley, New YorkGoogle Scholar
  154. Sutton R, Sposito G (2006) Molecular simulation of humic substance–Ca-montmorillonite complexes. Geochim Cosmochim Acta 70:3566–3581Google Scholar
  155. Trevisan S, Francioso O, Quaggiotti S, Nardi S (2010) Humic substances biological activity at the plant-soil interface. From environmental aspects to molecular factors. Plant Sign Behav 5:635–643Google Scholar
  156. Urrutia O, Erro J, Guardado I, San Francisco S, Mandado M, Baigorri R, Yvin J-C, Garcia-Mina JM (2014) Physico-chemical characterization of humic-metal-phosphate complexes and their potential application to the manufacture of new types of phosphate-based fertilizers. J Plant Nutr Soil Sci 177:128–136Google Scholar
  157. 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 Agric Food Chem 57:11267–11276PubMedGoogle Scholar
  158. Vaccaro S, Ertani A, Nebbioso A, Muscolo A, Quaggiotti S, Piccolo A, Nardi S (2015) Humic substances stimulate maize nitrogen assimilation and amino acid metabolism at physiological and molecular level. Chem Biol Technol Agric 2:5Google Scholar
  159. Varga B, Kiss G, Galambos I, Gelencser A, Hlavay J, Krivacsy Z (2000) Secondary structure of humic acids. Can micelle-like conformation be proved by aqueous size exclusion chromatography? Environ Sci Technol 34:3303–3306Google Scholar
  160. Ventorino V, De Marco A, Pepe O, Virzo De Santo A, Moschetti G (2012) Impact of innovative agricultural practices of carbon sequestration on soil microbial community. In: Piccolo A (ed) Carbon sequestration in agricultural soils. Springer-Verlag, Heidelberg, pp 145–177Google Scholar
  161. Vinci G, Cozzolino V, Mazzei P, Monda H, Spaccini R, Piccolo A (2018a) Effects of Bacillus amyloliquefaciens and organic and inorganic phosphate amendments on Maize plants as revealed by NMR and GC-MS based metabolomics. Plant Soil 429:1–14. Scholar
  162. Vinci G, Cozzolino V, Mazzei P, Monda H, Spaccini R, Piccolo A (2018b) An alternative to mineral phosphorus fertilizers: The combined effects of Trichoderma harzianum and compost on Zea mays, as revealed by 1H NMR and GC-MS metabolomics. Plos One (in press). Scholar
  163. Winkler A, Haumaier L, Zech W (2005) Insoluble alkyl carbon components in soils derive mainly from cutin and suberin. Org Geochem 36:519–529Google Scholar
  164. Woo DK, Quijano JC, Kumar P, Chaoka S, Bernacchi CJ (2014) Threshold dynamics in soil carbon storage for bioenergy crops. Environ Sci Technol 48:12090–12098PubMedGoogle Scholar
  165. Wood S, Baudron F (2018) Soil organic matter underlies crop nutritional quality and productivity in smallholder agriculture. Agric Ecosyst Environ 266:100–108Google Scholar
  166. Zancani M, Petrussa E, Krajňáková J, Casolo V, Spaccini R, Piccolo A, Macrì F, Vianello A (2009) Effect of humic acids on phosphate level and energetic metabolism of tobacco BY-2 suspension cell cultures. Env Exp Bot 65:287–295Google Scholar
  167. Zancani M, Bertolini A, Petrussa E, Krajňáková J, Piccolo A, Spaccini R, Vianello A (2011) Fulvic acid affects proliferation and maturation phases in Abies cephalonica embryogenic cells. J Plant Physiol 168:1226–1233PubMedGoogle Scholar
  168. Zheng Z, Zheng Y, Tian X, Yang Z, Jiang Y, Zhao F (2018) Interactions between iron mineral-humic complexes and hexavalent chromium and the corresponding bio-effects. Environ Pollut 241:265–271PubMedGoogle Scholar
  169. Zhou P, Pan GX, Spaccini R, Piccolo A (2010) Molecular changes in particulate organic matter (POM) in a typical Chinese paddy soil under different long-term fertilizer treatments. Eur J Soil Sci 61:231–242Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alessandro Piccolo
    • 1
    • 2
    Email author
  • Riccardo Spaccini
    • 1
    • 2
  • Davide Savy
    • 3
  • Marios Drosos
    • 4
  • Vincenza Cozzolino
    • 1
    • 2
  1. 1.Interdepartmental Research Centre on Nuclear Magnetic Resonance for the Environment, Agro-Food and New Materials (CERMANU)University of Napoli Federico IIPorticiItaly
  2. 2.Department of Agricultural SciencesUniversity of Napoli Federico IIPorticiItaly
  3. 3.Plant Biology LaboratoryUniversity of Liège, Gembloux Agro-Bio TechGemblouxBelgium
  4. 4.Faculty of Biology and EnvironmentInstitute of Resource, Ecosystem and Environment of Agriculture (IREEA), Nanjing Agricultural UniversityNanjingChina

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