Abstract
Evidence for a vital role of soil mineral matrix interactions in lipid preservation is steadily increasing. However, it remains unclear whether solvent-extractable (‘free’) or hydrolyzable (‘bound’) lipids, including molecular proxies, e.g., for cutin and suberin, are similarly affected by different stabilization mechanisms in soil (i.e., aggregation or organo-mineral association). To provide insights into the effect of these stabilization mechanisms on lipid composition and preservation, we investigated free and bound lipids in particulate and mineral soil fractions, deriving from sand- and silt-/clay-sized aggregates from a forest subsoil. While free lipids accumulated in sand-sized aggregates, the more complex bound lipids accumulated in silt- and clay-sized aggregates, particularly in the respective mineral fractions < 6.3 µm (fine silt and clay). The presence of both, cutin and suberin markers indicated input of leaf- and root-derived organic matter to the subsoil. Yet, our cutin marker (9,10,ω-trihydroxyoctadecanoic acid) was not extracted from the mineral aggregate compartments < 6.3 µm, perhaps due to its chemical structure (i.e., cross-linking via several hydroxy groups, and thus higher ‘stability’, in macromolecular structures). Combined, these results suggest that the chemical composition of lipids (and likely also that of other soil organic matter compounds) governs interaction with their environment, such as accumulation in aggregates or association with mineral soil compartments, and thus indirectly influences their persistence in soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andreetta A, Dignac MF, Carnicelli S (2013) Biological and physico-chemical processes influence cutin and suberin biomarker distribution in two Mediterranean forest soil profiles. Biogeochemistry 112:41–58. https://doi.org/10.1007/s10533-011-9693-9
Angst G, Heinrich L, Kögel-Knabner I, Mueller CW (2016a) The fate of cutin and suberin of decaying leaves, needles and roots—inferences from the initial decomposition of bound fatty acids. Org Geochem 95:81–92. https://doi.org/10.1016/j.orggeochem.2016.02.006
Angst G, John S, Mueller CW et al (2016b) Tracing the sources and spatial distribution of organic carbon in subsoils using a multi-biomarker approach. Sci Rep. https://doi.org/10.1038/srep29478
Angst G, Kögel-Knabner I, Kirfel K et al (2016c) Spatial distribution and chemical composition of soil organic matter fractions in rhizosphere and non-rhizosphere soil under European beech (Fagus sylvatica L.). Geoderma 264:179–187. https://doi.org/10.1016/j.geoderma.2015.10.016
Angst G, Cajthaml T, Angst Š et al (2017a) Performance of base hydrolysis methods in extracting bound lipids from plant material, soils, and sediments. Org Geochem. https://doi.org/10.1016/j.orggeochem.2017.08.004
Angst G, Mueller KE, Kögel-Knabner I et al (2017b) Aggregation controls the stability of lignin and lipids in clay-sized particulate and mineral associated organic matter. Biogeochemistry 132:307–324. https://doi.org/10.1007/s10533-017-0304-2
Baisden WT, Amundson R, Cook AC, Brenner DL (2002) Turnover and storage of C and N in five density fractions from California annual grassland surface soils. Glob Biogeochem Cycles 16(4):64-1–64-16
Bimüller C, Mueller CW, von Lützow M et al (2014) Decoupled carbon and nitrogen mineralization in soil particle size fractions of a forest topsoil. Soil Biol Biochem 78:263–273. https://doi.org/10.1016/j.soilbio.2014.08.001
Blankinship JC, Fonte SJ, Six J, Schimel JP (2016) Plant versus microbial controls on soil aggregate stability in a seasonally dry ecosystem. Geoderma 272:39–50. https://doi.org/10.1016/j.geoderma.2016.03.008
Bossuyt H, Six J, Hendrix PF (2005) Protection of soil carbon by microaggregates within earthworm casts. Soil Biol Biochem 37:251–258. https://doi.org/10.1016/j.soilbio.2004.07.035
Bridson JN (1985) Lipid fraction in forest litter: early stages of decomposition. Soil Biol Biochem 17:285–290. https://doi.org/10.1016/0038-0717(85)90062-8
Bull ID, Van Bergen PF, Nott CJ et al (2000) Organic geochemical studies of soils from the Rothamsted classical experiments-V. The fate of lipids in different long-term experiments. Org. Geochemistry 31:1367–1376
Chenu C, Plante ATF (2006) Clay-sized organo-mineral complexes in a cultivation chronosequence: revisiting the concept of the “primary organo-mineral complex”. Eur J Soil Sci 57:596–607. https://doi.org/10.1111/j.1365-2389.2006.00834.x
Cranwell PA (1981) Diagenesis of free and bound lipids in terrestrial detritus deposited in a lacustrine sediment. Org Geochem 3:79–89. https://doi.org/10.1016/0146-6380(81)90002-4
Crow SE, Swanston CW, Lajtha K et al (2007) Density fractionation of forest soils: methodological questions and interpretation of incubation results and turnover time in an ecosystem context. Biogeochemistry 85:69–90. https://doi.org/10.1007/s10533-007-9100-8
Diefendorf AF, Freeman KH, Wing SL, Graham HV (2011) Production of n-alkyl lipids in living plants and implications for the geologic past. Geochim Cosmochim Acta 75:7472–7485. https://doi.org/10.1016/j.gca.2011.09.028
Feng X, Xu Y, Jaffé R et al (2010) Turnover rates of hydrolysable aliphatic lipids in Duke Forest soils determined by compound specific 13C isotopic analysis. Org Geochem 41:573–579. https://doi.org/10.1016/j.orggeochem.2010.02.013
Filley TR, Boutton TW, Liao JD et al (2008) Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J Geophys Res Biogeosci. https://doi.org/10.1029/2007JG000564
Freimuth EJ, Diefendorf AF, Lowell TV (2017) Hydrogen isotopes of n-alkanes and n-alkanoic acids as tracers of precipitation in a temperate forest and implications for paleorecords. Geochim Cosmochim Acta 206:166–183. https://doi.org/10.1016/j.gca.2017.02.027
Funk DT (1990) Alnus glutionsa (L.) Gaertn., European alder. In: Silvics of North America. Washington DC
Gaudinski J, Trumbore S, Davidson E (2000) Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and partitioning of fluxes. Biogeochemistry 51:33–69. https://doi.org/10.1023/A:1006301010014
Gocke M, Kuzyakov Y, Wiesenberg GLB (2013) Differentiation of plant derived organic matter in soil, loess and rhizoliths based on n-alkane molecular proxies. Biogeochemistry 112:23–40. https://doi.org/10.1007/s10533-011-9659-y
Gonçalves CN, Dalmolin RSD, Dick DP et al (2003) The effect of 10% HF treatment on the resolution of CPMAS 13C NMR spectra and on the quality of organic matter in Ferralsols. Geoderma 116:373–392. https://doi.org/10.1016/S0016-7061(03)00119-8
Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307. https://doi.org/10.1016/j.scitotenv.2007.11.013
Griepentrog M, Eglinton TI, Hagedorn F et al (2015) Interactive effects of elevated CO2 and nitrogen deposition on fatty acid molecular and isotope composition of above- and belowground tree biomass and forest soil fractions. Glob Change Biol 21:473–486. https://doi.org/10.1111/gcb.12666
Guo M, Chorover J (2003) Transport and fractionation of dissolved organic matter in soil columns. Soil Sci 168:108–118. https://doi.org/10.1097/01.ss.0000055306.23789.65
Hernes PJ, Kaiser K, Dyda RY, Cerli C (2013) Molecular trickery in soil organic matter: hidden lignin. Environ Sci Technol 47:9077–9085. https://doi.org/10.1021/es401019n
Herold N, Scho I, Schrumpf M (2014) Controls on soil carbon storage and turnover in German landscapes. Biogeochemistry. https://doi.org/10.1007/s10533-014-9978-x
Jackson RB, Lajtha K, Crow SE et al (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol Syst. https://doi.org/10.1146/annurev-ecolsys-112414-054234
Jambu P, Fostec E, Jacquesy R (1978) Les lipides des sols: nature, origine, evolution, propriétés. Sci du Sol 4:229–240
Jansen B, Wiesenberg GLB (2017) Opportunities and limitations related to the application of plant-derived lipid molecular proxies in soil science. Soil. https://doi.org/10.5194/soil-2017-9
Jansen B, Nierop KGJ, Hageman JA et al (2006) The straight-chain lipid biomarker composition of plant species responsible for the dominant biomass production along two altitudinal transects in the Ecuadorian Andes. Org Geochem 37:1514–1536. https://doi.org/10.1016/j.orggeochem.2006.06.018
John B, Yamashita T, Ludwig B, Flessa H (2005) Storage of organic carbon in aggregate and density fractions of silty soils under different types of land use. Geoderma 128:63–79. https://doi.org/10.1016/j.geoderma.2004.12.013
Kaiser K, Zech W (1997) Competitive sorption of dissolved organic matter fractions to soils and related mineral phases. Soil Sci Soc Am J 61:64–69. https://doi.org/10.2136/sssaj1997.03615995006100010011x
Kaiser M, Berhe AA (2014) How does sonication affect the mineral and organic constituents of soil aggregates?-A review. J Plant Nutr Soil Sci 177:479–495. https://doi.org/10.1002/jpln.201300339
Kleber M, Mikutta R, Torn MS, Jahn R (2005) Poorly crystalline mineral phases protect organic matter in acid subsoil horizons. Eur J Soil Sci. https://doi.org/10.1111/j.1365-2389.2005.00706.x
Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162. https://doi.org/10.1016/S0038-0717(01)00158-4
Kolattukudy PE (1980) Bio-polyester membranes of plants—cutin and suberin. Science 208(80):990–1000. https://doi.org/10.1126/science.208.4447.990
Kölbl A, Leifeld J, Kögel-Knabner I (2005) A comparison of two methods for the isolation of free and occluded particulate organic matter. J Plant Nutr Soil Sci 168:660–667. https://doi.org/10.1002/jpln.200521805
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. https://doi.org/10.1038/nature16069
Li FF, Zhang PC, Wu DP et al (2017) Acid pretreatment increased lipid biomarker extractability: a case study to reveal soil organic matter input from rubber trees after long-term cultivation. Eur J Soil Sci. https://doi.org/10.1111/ejss.12501
Liang C, Balser TC (2008) Preferential sequestration of microbial carbon in subsoils of a glacial-landscape toposequence, Dane County, WI, USA. Geoderma 148:113–119. https://doi.org/10.1016/j.geoderma.2008.09.012
Lichtfouse É, Berthier G, Houot S et al (1995) Stable carbon isotope evidence for the microbial origin of C14-C18 n-alkanoic acids in soils. Org Geochem 23:849–852. https://doi.org/10.1016/0146-6380(95)80006-D
Lin LH, Simpson MJ (2016) Enhanced extractability of cutin- and suberin-derived organic matter with demineralization implies physical protection over chemical recalcitrance in soil. Org Geochem 97:111–121. https://doi.org/10.1016/j.orggeochem.2016.04.012
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
Meyers PA, Ishiwatari R (1993) Lacustrine organic geochemistry-an overview of indicators of organic matter sources and diagenesis in lake sediments. Org Geochem 20:867–900. https://doi.org/10.1016/0146-6380(93)90100-P
Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56. https://doi.org/10.1007/s10533-005-0712-6
Monreal CM, Schulten HR, Kodama H (1997) Age, turnover and molecular diversity of soil organic matter in aggregates of a Gleysol. Can J Soil Sci 77:379–388. https://doi.org/10.4141/S95-064
Mueller CW, Bruggemann N, Pritsch K et al (2009) Initial differentiation of vertical soil organic matter distribution and composition under juvenile beech (Fagus sylvatica L.) trees. Plant Soil 323:111–123. https://doi.org/10.1007/s11104-009-9932-1
Mueller KE, Polissar PJ, Oleksyn J, Freeman KH (2012) Differentiating temperate tree species and their organs using lipid biomarkers in leaves, roots and soil. Org Geochem 52:130–141. https://doi.org/10.1016/j.orggeochem.2012.08.014
Mueller KE, Eissenstat DM, Muller CW et al (2013) What controls the concentration of various aliphatic lipids in soil? Soil Biol Biochem 63:14–17. https://doi.org/10.1016/j.soilbio.2013.03.021
Mueller CW, Gutsch M, Kothieringer K et al (2014) Bioavailability and isotopic composition of CO2 released from incubated soil organic matter fractions. Soil Biol Biochem 69:168–178
Naafs DFW, Van Bergen PF, Boogert SJ, De Leeuw JW (2004a) Solvent-extractable lipids in an acid andic forest soil; variations with depth and season. Soil Biol Biochem 36:297–308. https://doi.org/10.1016/j.soilbio.2003.10.005
Naafs DFW, Van Bergen PF, De Jong MA et al (2004b) Total lipid extracts from characteristic soil horizons in a podzol profile. Eur J Soil Sci 55:657–669. https://doi.org/10.1111/j.1365-2389.2004.00633.x
Naafs DFW, Nierop KGJ, van Bergen PF, de Leeuw JW (2005) Changes in the molecular composition of ester-bound aliphatics with depth in an acid andic forest soil. Geoderma 127:130–136. https://doi.org/10.1016/j.geoderma.2004.11.022
Nierop KGJ (1998) Origin of aliphatic compounds in a forest soil. Org Geochem 29:1009–1016. https://doi.org/10.1016/S0146-6380(98)00165-X
Nierop KGJ, Verstraten JM (2004) Rapid molecular assessment of the bioturbation extent in sandy soil horizons under, pine using ester-bound lipids by on-line thermally assisted hydrolysis and methylation-gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 18:1081–1088. https://doi.org/10.1002/rcm.1449
Nierop KGJ, Naafs DFW, Verstraten JM (2003) Occurrence and distribution of ester-bound lipids in Dutch coastal dune soils along a pH gradient. Org Geochem 34:719–729. https://doi.org/10.1016/s0146-6380(03)00042-1
Nierop KGJ, Naafs DFW, Van Bergen PF (2005) Origin, occurrence and fate of extractable lipids in Dutch coastal dune soils along a pH gradient. Org Geochem 36:555–566. https://doi.org/10.1016/j.orggeochem.2004.11.003
Nierop KGJ, Jansen B, Hageman JA, Verstraten JM (2006) The complementarity of extractable and ester-bound lipids in a soil profile under pine. Plant Soil 286:269–285. https://doi.org/10.1007/s11104-006-9043-1
Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337. https://doi.org/10.1007/bf02205590
Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815. https://doi.org/10.1071/sr9910815
Otto A, Simpson MJ (2006) Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org Geochem 37:385–407. https://doi.org/10.1016/j.orggeochem.2005.12.011
Pisani O, Hills KM, Courtier-Murias D et al (2013) Molecular level analysis of long term vegetative shifts and relationships to soil organic matter composition. Org Geochem 62:7–16. https://doi.org/10.1016/j.orggeochem.2013.06.010
Pisani O, Frey SD, Simpson AJ, Simpson MJ (2015) Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry 123:391–409. https://doi.org/10.1007/s10533-015-0073-8
Plaza C, Fernández JM, Pereira EIP, Polo A (2012) A comprehensive method for fractionating soil organic matter not protected and protected from decomposition by physical and chemical mechanisms. Clean—Soil, Air, Water 40:134–139. https://doi.org/10.1002/clen.201100338
Poeplau C, Don A (2013) Sensitivity of soil organic carbon stocks and fractions to different land-use changes across Europe. Geoderma 192:189–201. https://doi.org/10.1016/j.geoderma.2012.08.003
Poirier N, Sohi SP, Gaunt JL et al (2005) The chemical composition of measurable soil organic matter pools. Org Geochem 36:1174–1189. https://doi.org/10.1016/j.orggeochem.2005.03.005
Puget P, Chenu C, Balesdent J (2000) Dynamics of soil organic matter associated with particle-size fractions of water-stable aggregates. Eur J Soil Sci 51:595–605. https://doi.org/10.1046/j.1365-2389.2000.00353.x
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rasse DP, Rumpel C, Dignac M-FF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. https://doi.org/10.1007/s11104-004-0907-y
Riederer M, Matzke K, Ziegler F, Kögel-Knabner I (1993) Occurence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org Geochem 20:1063–1076. https://doi.org/10.1016/0146-6380(93)90114-q
Rumpel C, Rabia N, Derenne S et al (2006) Alteration of soil organic matter following treatment with hydrofluoric acid (HF). Org Geochem 37:1437–1451. https://doi.org/10.1016/j.orggeochem.2006.07.001
Schmidt MWI, Knicker H, Hatcher PG, Kögel-Knabner I (1997) Improvement of 13C and 15N CPMAS NMR spectra of bulk soils, particle size fractions and organic material by treatment with 10% hydrofluoric acid. Eur J Soil Sci 48:319–328. https://doi.org/10.1111/j.1365-2389.1997.tb00552.x
Six J, Callewaert P, Lenders S et al (2002) Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Sci Soc Am J 66:1981–1987
Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31. https://doi.org/10.1016/j.still.2004.03.008
Sollins P, Kramer MG, Swanston C et al (2009) Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231. https://doi.org/10.1007/s10533-009-9359-z
State Administration of Land Surveying and Cadastre (2018) ČÚZK: geoportal. http://geoportal.cuzk.cz/geoprohlizec. Accessed 6 Aug 2018
Trivedi P, Rochester IJ, Trivedi C et al (2015) Soil aggregate size mediates the impacts of cropping regimes on soil carbon and microbial communities. Soil Biol Biochem 91:169–181. https://doi.org/10.1016/j.soilbio.2015.08.034
van Bergen PF, Nott CJ, Bull ID et al (1998) Organic geochemical studies of soils from the Rothamsted classical experiments—IV. Preliminary results from a study of the effect of soil pH on organic matter decay. Org Geochem 29:1779–1795. https://doi.org/10.1016/S0146-6380(98)00188-0
Van der Voort TS, Zell CI, Hagedorn F et al (2017) Diverse soil carbon dynamics expressed at the molecular level. Geophys Res Lett. https://doi.org/10.1002/2017GL076188
Virto I, Barré P, Chenu C (2008) Microaggregation and organic matter storage at the silt-size scale. Geoderma 146:326–335. https://doi.org/10.1016/j.geoderma.2008.05.021
von Lützow M, Kögel-Knabner I, Ekschmitt K et al (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445. https://doi.org/10.1111/j.1365-2389.2006.00809.x
von Lützow M, Kögel-Knabner I, Ekschmitt K et al (2007) SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207. https://doi.org/10.1016/j.soilbio.2007.03.007
Wagai R, Mayer LM, Kitayama K (2009) Nature of the “occluded” low-density fraction in soil organic matter studies: a critical review. Soil Sci Plant Nutr 55:13–25. https://doi.org/10.1111/j.1747-0765.2008.00356.x
Wallander H, Mörth CM, Giesler R (2009) Increasing abundance of soil fungi is a driver for 15N enrichment in soil profiles along a chronosequence undergoing isostatic rebound in northern Sweden. Oecologia 160:87–96. https://doi.org/10.1007/s00442-008-1270-0
Wiesenberg GLB, Dorodnikov M, Kuzyakov Y (2010a) Source determination of lipids in bulk soil and soil density fractions after four years of wheat cropping. Geoderma 156:267–277. https://doi.org/10.1016/j.geoderma.2010.02.026
Wiesenberg GLB, Gocke M, Kuzyakov Y (2010b) Fast incorporation of root-derived lipids and fatty acids into soil—evidence from a short term multiple pulse labelling experiment. Org Geochem 41:1049–1055. https://doi.org/10.1016/j.orggeochem.2009.12.007
Yavitt JB, Fahey TJ, Sherman RE, Groffman PM (2015) Lumbricid earthworm effects on incorporation of root and leaf litter into aggregates in a forest soil, New York State. Biogeochemistry 125:261–273. https://doi.org/10.1007/s10533-015-0126-z
Acknowledgements
This work was realized within the Program for Research and Mobility Support of Starting Researchers of the Czech Academy of Sciences (Grant Number MSM200961705) and with support of MEYS CZ Grant Numbers: LM2015075 and EF16_013/0001782 – SoWa Ecosystems Research, and the Czech Science Foundation (Grant 18-24138S). We would like to thank Petr Kotas for support in chromatogram evaluation, Tomáš Picek for help with sample preparation, Anita van Leeuwen-Tolboom for XRD measurements, and Katja Heister and Francien Peterse for facilitating the Geolab infrastructure in Utrecht.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Asmeret Asefaw Berhe.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Angst, G., Nierop, K.G.J., Angst, Š. et al. Abundance of lipids in differently sized aggregates depends on their chemical composition. Biogeochemistry 140, 111–125 (2018). https://doi.org/10.1007/s10533-018-0481-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-018-0481-7