Advertisement

Biogeochemistry

, Volume 142, Issue 1, pp 117–135 | Cite as

Consistent proteinaceous organic matter partitioning into mineral and organic soil fractions during pedogenesis in diverse ecosystems

  • Jinyoung Moon
  • Kang Xia
  • Mark A. WilliamsEmail author
Article
  • 138 Downloads

Abstract

Proteinaceous compounds are critical in soil organic matter (SOM) formation and persistence, but the partitioning into mineral-associated and organic forms during hundreds and thousands of years of pedogenesis are poorly understood across multiple climates and vegetation types. We investigated the partitioning of amino acids (AA) into mineral-bound (MB) and non-mineral associated organic (NMO) soil fractions to discern whether consistent patterns during ecosystem development were observed across two different climates (cool temperate continental, USA; and moist oceanic forests, New Zealand). Although each ecosystem retained unique soil AA signatures, consistent patterns in both systems were observed with three main findings. (1) Regardless of differences in climate and vegetation between the two ecosystems, AA consistently partitioned in similar ways into MB and NMO soil fractions. For example, Thr, Ser, and Asx were relatively more dominant in the NMO fraction while Arg, Lys, Cys, and Met were relatively more dominant in the MB soil fraction. (2) AA change, showed similar trends related to chemical groupings of positively-charged, polar aromatic, sulfur containing, and non-polar AAs across both ecosystems consistent with changing patterns of soil Fe and Al bearing minerals, such as an increasing weathering index (WI; Fe dithionite/total Fe) and losses of Fe and Al from surface soils during ecosystem development. (3) The pedogenic patterns of AA change, in each system paralleled biological transitions in bacterial communities, suggesting a linkage between the AA sources and the soil sink that contributes to soil organic N. This latter point contrasts with the potential for complete change in soil AA composition that could occur upon processing and binding in soil. Overall, the consistency in the types of AAs that partition into either MB or NMO soil fractions across locations provide evidence of similar processes that contribute to soil organic N accrual across soils. Some AA also appeared to be retained in soil by electrostatic forces, and AA–organic matter interactions, that need further study. Mineral–metal complexation of AAs with sulfur side chain groups, and non-polar interactions, respectively, provide examples of these potential mechanisms for study. The results not only support mechanisms of soil proteinacous organic matter chemistry being driven by the interactions with the soil matrix, acting as a “sink”, but also draw attention to the sources of organic matter (microbes, plants) in determining the composition of organic N in soil during pedogenesis.

Keywords

Soil organic matter Microbial Amino acids Proteinaceous Plant Chronosequence Mineral 

Abbreviations

AA

Amino acid

SOM

Soil organic matter

OM

Organic matter

SON

Soil organic nitrogen

WI

Weathering index

NMO

Non-mineral associated organic

MB

Mineral-bound

Notes

Acknowledgements

This research was funded by the United States Department of Agriculture National Institute of Food and Agriculture Foundational Programs (grant# 2011-03815). We acknowledge the DNR of the state of Michigan, Dr. Shankar G. Shanmugam for collecting soil samples from Lake Michigan chronosequence, Dr. Madhavi L. Kakumanu for the density fractionation of soils, Dr. Chao Shang for technical advice on the HPLC instrumentation, and Thurman Haynes for extraction of soil Fe and Al mineral fractions.

Supplementary material

10533_2018_523_MOESM1_ESM.docx (788 kb)
Supplementary material 1 (DOCX 789 kb)

References

  1. Abe T, Watanabe A (2004) X-ray photoelectron spectroscopy of nitrogen functional groups in soil humic acids. Soil Sci 169:35–43.  https://doi.org/10.1097/01.ss.0000112016.97541.28 CrossRefGoogle Scholar
  2. Ahmed AA, Thiele-Bruhn S, Aziz SG et al (2015) Interaction of polar and nonpolar organic pollutants with soil organic matter: sorption experiments and molecular dynamics simulation. Sci Tot Environ 508:276–287CrossRefGoogle Scholar
  3. Allard B (2006) A comparative study on the chemical composition of humic acids from forest soil, agricultural soil and lignite deposit: bound lipid, carbohydrate and amino acid distributions. Geoderma 130:77–96.  https://doi.org/10.1016/j.geoderma.2005.01.010 CrossRefGoogle Scholar
  4. Amelung W (2003) Nitrogen biomarkers and their fate in soil. J Plant Nutr Soil Sci 166:677–686.  https://doi.org/10.1002/jpln.200321274 CrossRefGoogle Scholar
  5. Amelung W, Zhang X (2001) Determination of amino acid enantiomers in soils. Soil Biol Biochem 33:553–562.  https://doi.org/10.1016/S0038-0717(00)00195-4 CrossRefGoogle Scholar
  6. Amelung W, Brodowski S, Sandhage-Hofmann A, Bol R (2008) Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter. Elsevier, San Diego, pp 155–250Google Scholar
  7. Betts MJ, Russell RB (2003) Amino acid properties and consequences of substitutions. Bioinform Genet 317:289CrossRefGoogle Scholar
  8. Bol R, Poirier N, Balesdent J, Gleixner G (2009) Molecular turnover time of soil organic matter in particle-size fractions of an arable soil. Rapid Commun Mass Spectrom 23:2551–2558CrossRefGoogle Scholar
  9. Bosch L, Alegría A, Farré R (2006) Application of the 6-aminoquinolyl-N-hydroxysccinimidyl carbamate (AQC) reagent to the RP-HPLC determination of amino acids in infant foods. J Chromatogr B 831:176–183.  https://doi.org/10.1016/j.jchromb.2005.12.002 CrossRefGoogle Scholar
  10. Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136:1636S–1640SCrossRefGoogle Scholar
  11. Buol SW, Southard RJ, Graham RC, McDaniel PA (2011) Soil genesis and classification. Wiley, ChichesterCrossRefGoogle Scholar
  12. Chen W, Shao Y, Chen F (2013) Evolution of complete proteomes: guanine-cytosine pressure, phylogeny and environmental influences blend the proteomic architecture. BMC Evol Biol 13:219CrossRefGoogle Scholar
  13. Chenu C, Angers DA, Barré P et al (2018) Increasing organic stocks in agricultural soils: knowledge gaps and potential innovations. Soil Tillage Res.  https://doi.org/10.1016/j.still.2018.04.011 Google Scholar
  14. DiCosty RJ, Weliky DP, Anderson SJ, Paul EA (2003) 15N-CPMAS nuclear magnetic resonance spectroscopy and biological stability of soil organic nitrogen in whole soil and particle-size fractions. Org Geochem 34:1635–1650.  https://doi.org/10.1016/j.orggeochem.2003.08.005 CrossRefGoogle Scholar
  15. Dümig A, Häusler W, Steffens M, Kögel-Knabner I (2012) Clay fractions from a soil chronosequence after glacier retreat reveal the initial evolution of organo-mineral associations. Geochim Cosmochim Acta 85:1–18.  https://doi.org/10.1016/j.gca.2012.01.046 CrossRefGoogle Scholar
  16. Eger A, Almond PC, Condron LM (2011) Pedogenesis, soil mass balance, phosphorus dynamics and vegetation communities across a Holocene soil chronosequence in a super-humid climate, South Westland, New Zealand. Geoderma 163:185–196CrossRefGoogle Scholar
  17. Fan T, Lane AN, Chekmenev E et al (2004) Synthesis and physico-chemical properties of peptides in soil humic substances. J Pept Res 63:253–264CrossRefGoogle Scholar
  18. Friedel JK, Scheller E (2002) Composition of hydrolysable amino acids in soil organic matter and soil microbial biomass. Soil Biol Biochem 34(3):315–325.  https://doi.org/10.1016/S0038-0717(01)00185-7 CrossRefGoogle Scholar
  19. Gärdenäs AI, Ågren GI, Bird JA et al (2011) Knowledge gaps in soil carbon and nitrogen interactions—from molecular to global scale. Soil Biol Biochem 43:702–717.  https://doi.org/10.1016/j.soilbio.2010.04.006 CrossRefGoogle Scholar
  20. Glaser B, Amelung W (2002) Determination of 13C natural abundance of amino acid enantiomers in soil: methodological considerations and first results. Rapid Commun Mass Spectrom 16:891–898.  https://doi.org/10.1002/rcm.650 CrossRefGoogle Scholar
  21. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Tot Environ 404:297–307.  https://doi.org/10.1016/j.scitotenv.2007.11.013 CrossRefGoogle Scholar
  22. Hobara S, Osono T, Hirose D et al (2014) The roles of microorganisms in litter decomposition and soil formation. Biogeochemistry 118:471–486CrossRefGoogle Scholar
  23. Hou S, He H, Zhang X et al (2009) Determination of soil amino acids by high performance liquid chromatography-electro spray ionization-mass spectrometry derivatized with 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate. Talanta 80:440–447.  https://doi.org/10.1016/j.talanta.2009.07.013 CrossRefGoogle Scholar
  24. Huntjens JLM (1972) Amino acid composition of humic acid-like polymers produced by streptomycetes and of humic acids from pasture and arable land. Soil Biol Biochem 4:339–345.  https://doi.org/10.1016/0038-0717(72)90030-2 CrossRefGoogle Scholar
  25. Jangid K, Whitman WB, Condron LM et al (2013) Progressive and retrogressive ecosystem development coincide with soil bacterial community change in a dune system under lowland temperate rainforest in New Zealand. Plant Soil 367(1–2):235–247CrossRefGoogle Scholar
  26. Jaworska H, Dąbkowska-Naskręt H, Kobierski M (2016) Iron oxides as weathering indicator and the origin of Luvisols from the Vistula glaciation region in Poland. J Soils Sediments 16:396–404CrossRefGoogle Scholar
  27. Jenkinson DS, Coleman K (2008) The turnover of organic carbon in subsoils. Part 2. Modelling carbon turnover. Eur J Soil Sci 59:400–413.  https://doi.org/10.1111/j.1365-2389.2008.01026.x CrossRefGoogle Scholar
  28. 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 85:9–24.  https://doi.org/10.1007/s10533-007-9103-5 CrossRefGoogle Scholar
  29. Knicker H (2011) Soil organic N - An under-rated player for C sequestration in soils? Soil Biol Biochem 43:1118–1129.  https://doi.org/10.1016/j.soilbio.2011.02.020 CrossRefGoogle Scholar
  30. Knicker H, Hatcher PG (1997) Survival of protein in an organic-rich sediment: possible protection by encapsulation in organic matter. Naturwissenschaften 84:231–234.  https://doi.org/10.1007/s001140050384 CrossRefGoogle Scholar
  31. Koch AL (2006) The bacteria: their origin, structure, function and antibiosis. Springer, BerlinCrossRefGoogle Scholar
  32. Kögel-Knabner I, Guggenberger G, Kleber M, Kandeler E, Kalbitz K, Scheu S, Eusterhues K, Leinweber P (2008) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171(1):61–82CrossRefGoogle Scholar
  33. Kramer MG, Sanderman J, Chadwick OA et al (2012) Long-term carbon storage through retention of dissolved aromatic acids by reactive particles in soil. Glob Chang Biol 18:2594–2605CrossRefGoogle Scholar
  34. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132.  https://doi.org/10.1016/0022-2836(82)90515-0 CrossRefGoogle Scholar
  35. Leinemann T, Preusser S, Mikutta R, Kalbitz K et al (2018) Multiple exchange processes on mineral surfaces control the transport of dissolved organic matter through soil profiles. Soil Biol Biochem 118:79–90CrossRefGoogle Scholar
  36. Leinweber P, Kruse J, Baum C et al (2013) Advances in understanding organic nitrogen chemistry in soils using state-of-the-art analytical techniques. Adv Agron 119:e151Google Scholar
  37. Lichter J (1995a) Mechanisms of plant succession in coastal Lake Michigan sand dunes. University of Minnesota, MinneapolisGoogle Scholar
  38. Lichter J (1995b) Lake Michigan beach-ridge and dune development, lake level, and variability in regional water balance. Quat Res 44:181–189CrossRefGoogle Scholar
  39. Lichter J (1998) Rates of weathering and chemical depletion in soils across a chronosequence of Lake Michigan sand dunes. Geoderma 85:255–282CrossRefGoogle Scholar
  40. Lowe LE (1973) Amino acid distribution in forest humus layers in British Columbia. Soil Sci Soc Am J 37:569–572CrossRefGoogle Scholar
  41. Ma L (2015) Soil organic nitrogen—investigation of soil amino acids and proteinaceous compounds. Doctoral DissertationsGoogle Scholar
  42. Marschner B, Brodowski S, Dreves A et al (2008) How relevant is recalcitrance for the stabilization of organic matter in soils? J Plant Nutr Soil Sci 171:91–110.  https://doi.org/10.1002/jpln.200700049 CrossRefGoogle Scholar
  43. Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472.  https://doi.org/10.2307/1936576 CrossRefGoogle Scholar
  44. Mikutta R, Kaiser K, Dörr N et al (2010) Mineralogical impact on organic nitrogen across a long-term soil chronosequence (0.3–4100 kyr). Geochim Cosmochim Acta 74:2142–2164.  https://doi.org/10.1016/j.gca.2010.01.006 CrossRefGoogle Scholar
  45. Moon J (2015) Selective accrual and dynamics of proteinaceous compounds during pedogenesis: testing source and sink selection hypotheses. Virginia Tech, BlacksburgGoogle Scholar
  46. Moon J, Ma L, Xia K, Williams MA (2016) Plant–Microbial and mineral contributions to amino acid and protein organic matter accumulation during 4000 years of pedogenesis. Soil Biol Biochem 100:42–50.  https://doi.org/10.1016/j.soilbio.2016.05.011 CrossRefGoogle Scholar
  47. Palmer RWP, Doyle RB, Grealish GJ, Almond PC (1985) Soil studies in South Westland 1984/1985. Soil Bureau District Office Report NP 2. Department of Scientific and Industrial Research, New ZealandGoogle Scholar
  48. Parton WJ, Ojima DS, Schimel DS, Kittel TGF (1992) Development of simplified ecosystem models for applications in Earth system studies: The Century experience. In: Ojima DS (ed) Modeling the earth system. Proceedings from the 1990 Global Change Institute on Earth System Modeling, 16–27 July 1990. Aspen Global Change Institute, AspenGoogle Scholar
  49. Philben M, Ziegler SE, Edwards KA et al (2016) Soil organic nitrogen cycling increases with temperature and precipitation along a boreal forest latitudinal transect. Biogeochemistry 127:397–410.  https://doi.org/10.1007/s10533-016-0187-7 CrossRefGoogle Scholar
  50. Rasmussen C, Heckman K, Wieder WR, Keiluweit M et al (2018) Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137(3):297–306CrossRefGoogle Scholar
  51. Poirier N, Sohi SP, Gaunt JL, Mahieu N, Randall EW, Powlson DS, Evershed RP (2005) The chemical composition of measurable soil organic matter pools. Org Geochem 36(8):1174–1189CrossRefGoogle Scholar
  52. Rattenbury MS, Jongens R, Cox SC (2010) Geology of the Haast Area. Institute of Geological & Nuclear Sciences 1: 250,000 Geological Map 14. GNS Science Lower HuttGoogle Scholar
  53. Rothstein DE (2009) Soil amino-acid availability across a temperate-forest fertility gradient. Biogeochemistry 92:201–215CrossRefGoogle Scholar
  54. Rothstein DE (2010) Effects of amino-acid chemistry and soil properties on the behavior of free amino acids in acidic forest soils. Soil Biol Biochem 42:1743–1750.  https://doi.org/10.1016/j.soilbio.2010.06.011 CrossRefGoogle Scholar
  55. Rovira P, Fernàndez P, Coûteaux M, Ramón VV (2005) Changes in the amino acid composition of decomposing plant materials in soil: species and depth effects. Commun Soil Sci Plant Anal 36:2933–2950.  https://doi.org/10.1080/00103620500306122 CrossRefGoogle Scholar
  56. Rovira P, Kurz-Besson C, Hernàndez P et al (2008) Searching for an indicator of N evolution during organic matter decomposition based on amino acids behaviour: a study on litter layers of pine forests. Plant Soil 307:149–166.  https://doi.org/10.1007/s11104-008-9592-6 CrossRefGoogle Scholar
  57. Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56CrossRefGoogle Scholar
  58. Schulten H-R, Schnitzer M (1998) The chemistry of soil organic nitrogen: a review. Biol Fertil Soils 26:1–15.  https://doi.org/10.1007/s003740050335 CrossRefGoogle Scholar
  59. Senesi N, Xing B, Huang PM (2009) Biophysico-chemical processes involving natural nonliving organic matter in environmental systems. Wiley, HobokenCrossRefGoogle Scholar
  60. Sollins P, Swanston C, Kleber M et al (2006) Organic C and N stabilization in a forest soil: evidence from sequential density fractionation. Soil Biol Biochem 38:3313–3324.  https://doi.org/10.1016/j.soilbio.2006.04.014 CrossRefGoogle Scholar
  61. Stevenson FJ (1982) Organic forms of soil nitrogen. In: Stevenson FJ (ed) Nitrogen in agricultural soils. American Society of Agronomy, Madison, pp 101–104Google Scholar
  62. Strahm BD, Harrison RB (2008) Controls on the sorption, desorption and mineralization of low-molecular-weight organic acids in variable-charge soils. Soil Sci Soc Am J 72:1653.  https://doi.org/10.2136/sssaj2007.0318 CrossRefGoogle Scholar
  63. Turner S, Meyer-Stüve S, Schippers A, Guggenberger G, Schaarschmidt F, Wild B, Richter A, Dohrmann R, Mikutta R (2017) Microbial utilization of mineral-associated nitrogen in soils. Soil Biol Biochem 104:185–196CrossRefGoogle Scholar
  64. Turner BL, Wells A, Andersen KM, Condron LM (2012) Patterns of tree community composition along a coastal dune chronosequence in lowland temperate rain forest in New Zealand. Plant Ecol 213:1525–1541.  https://doi.org/10.1007/s11258-012-0108-3 CrossRefGoogle Scholar
  65. Vieublé Gonod L, Jones DL, Chenu C (2006) Sorption regulates the fate of the amino acids lysine and leucine in soil aggregates. Eur J Soil Sci 57:320–329.  https://doi.org/10.1111/j.1365-2389.2005.00744.x CrossRefGoogle Scholar
  66. Vranova V, Zahradnickova H, Janous D et al (2012) The significance of D-amino acids in soil, fate and utilization by microbes and plants: review and identification of knowledge gaps. Plant Soil 354:21–39.  https://doi.org/10.1007/s11104-011-1059-5 CrossRefGoogle Scholar
  67. Wagner GH, Mutatkar VK (1968) Amino components of soil organic matter formed during humification of 14C Glucose1. Soil Sci Soc Am J 32:683.  https://doi.org/10.2136/sssaj1968.03615995003200050030x CrossRefGoogle Scholar
  68. Werdin-Pfisterer NR, Kielland K, Boone RD (2009) Soil amino acid composition across a boreal forest successional sequence. Soil Biol Biochem 41:1210–1220.  https://doi.org/10.1016/j.soilbio.2009.03.001 CrossRefGoogle Scholar
  69. Williams MA, Jangid K, Shanmugam SG, Whitman WB (2013) Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons. Soil Biol Biochem 57:749.  https://doi.org/10.1016/j.soilbio.2012.08.023 CrossRefGoogle Scholar
  70. Young RB, Avneri-Katz S, McKenna AM et al (2018) Composition-dependent sorptive fractionation of anthropogenic dissolved organic matter by Fe(III)-montmorillonite. Soil Systems 2(1):14CrossRefGoogle Scholar
  71. Zang X, van Heemst JDH, Dria KJ, Hatcher PG (2000) Encapsulation of protein in humic acid from a histosol as an explanation for the occurrence of organic nitrogen in soil and sediment. Org Geochem 31:679–695.  https://doi.org/10.1016/S0146-6380(00)00040-1 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.School of Plant and Environmental SciencesVirginia Polytechnic Institute & State UniversityBlacksburgUSA

Personalised recommendations