Abstract
Soil organic matter (SOM) often increases with the abundance of short-range-ordered iron (SRO Fe) mineral phases at local to global scales, implying a protective role for SRO Fe. However, less is known about how Fe phase composition and crystal order relate to SOM composition and turnover, which could be linked to redox alteration of Fe phases. We tested the hypothesis that the composition and turnover of mineral-associated SOM co-varied with Fe phase crystallinity and abundance across a well-characterized catena in the Luquillo Experimental Forest, Puerto Rico, using dense fractions from 30 A and B horizon soil samples. The δ13C and δ15N values of dense fractions were strongly and positively correlated (R2 = 0.75), indicating microbial transformation of plant residues with lower δ13C and δ15N values. However, comparisons of dense fraction isotope ratios with roots and particulate matter suggested a greater contribution of plant versus microbial biomass to dense fraction SOM in valleys than ridges. Similarly, diffuse reflectance infrared Fourier transform spectroscopy indicated that SOM functional groups varied significantly along the catena. These trends in dense fraction SOM composition, as well as ∆14C values indicative of turnover rates, were significantly related to Fe phase crystallinity and abundance quantified with selective extractions. Mössbauer spectroscopy conducted on independent bulk soil samples indicated that nanoscale ordered Fe oxyhydroxide phases (nano-goethite, ferrihydrite, and/or very-SRO Fe with high substitutions) dominated (66–94%) total Fe at all positions and depths, with minor additional contributions from hematite, silicate and adsorbed FeII, and ilmenite. An additional phase that could represent organic-FeIII complexes or aluminosilicate-bearing FeIII was most abundant in valley soils (17–26% of total Fe). Overall, dense fraction samples with increasingly disordered Fe phases were significantly associated with increasingly plant-derived and faster-cycling SOM, while samples with relatively more-crystalline Fe phases tended towards slower-cycling SOM with a greater microbial component. Our data suggest that counter to prevailing thought, increased SRO Fe phase abundance in dynamic redox environments could facilitate transient accumulation of litter derivatives while not necessarily promoting long-term C stabilization.
Similar content being viewed by others
References
Assis CP, Jucksch I, Mendonça ES et al (2012) Distribution and quality of the organic matter in light and heavy fractions of a red Latosol under different uses and management practices. Commun Soil Sci Plant Anal 43:835–846. https://doi.org/10.1080/00103624.2012.648469
Barcellos D, Cyle KT, Thompson A (2018) Faster redox fluctuations can lead to higher iron reduction rates in humid forest soils. Biogeochemistry 137:367–378. https://doi.org/10.1007/s10533-018-0427-0
Baumann K, Schöning I, Schrumpf M et al (2016) Rapid assessment of soil organic matter: soil color analysis and Fourier transform infrared spectroscopy. Geoderma 278:49–57. https://doi.org/10.1016/j.geoderma.2016.05.012
Berhe AA, Harden JW, Torn MS et al (2012a) Persistence of soil organic matter in eroding versus depositional landform positions. J Geophys Res Biogeosci 117:G02019. https://doi.org/10.1029/2011JG001790
Berhe AA, Suttle KB, Burton SD, Banfield JF (2012b) Contingency in the direction and mechanics of soil organic matter responses to increased rainfall. Plant Soil 358:371–383. https://doi.org/10.1007/s11104-012-1156-0
Blume HP, Schwertmann U (1969) Genetic evaluation of profile distribution of aluminum, iron, and manganese oxides. Soil Sci Soc Am J 33:438–444
Bonneville S, Behrends T, Van Cappellen P (2009) Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: a linear free energy relationship. Geochim Cosmochim Acta 73:5273–5282. https://doi.org/10.1016/j.gca.2009.06.006
Buettner SW, Kramer MG, Chadwick OA, Thompson A (2014) Mobilization of colloidal carbon during iron reduction in basaltic soils. Geoderma 221–222:139–145. https://doi.org/10.1016/j.geoderma.2014.01.012
Buss HL, Chapela Lara M, Moore OW et al (2017) Lithological influences on contemporary and long-term regolith weathering at the Luquillo Critical Zone Observatory. Geochim Cosmochim Acta 196:224–251. https://doi.org/10.1016/j.gca.2016.09.038
Celi L, Schnitzer M, Nègre M (1997) Analysis of carboxyl groups in soil humic acids by a wet chemical method, Fourier-transform infrared spectrometry and solution-state carbon-13 nuclear magnetic resonance. A comparative study. Soil Sci 162:189–197. https://doi.org/10.1097/00010694-199703000-00004
Chen C, Thompson A (2018) Ferrous iron oxidation under varying pO2 levels: the effect of Fe(III)/Al(III) oxide minerals and organic matter. Environ Sci Technol 52:597–606. https://doi.org/10.1021/acs.est.7b05102
Chen C, Dynes JJ, Wang J, Sparks DL (2014) Properties of Fe-organic matter associations via coprecipitation versus adsorption. Environ Sci Technol 48:13751–13759. https://doi.org/10.1021/es503669u
Chorover J, Amistadi MK (2001) Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim Cosmochim Acta 65:95–109. https://doi.org/10.1016/S0016-7037(00)00511-1
Chorover J, Amistadi MK, Chadwick OA (2004) Surface charge evolution of mineral-organic complexes during pedogenesis in Hawaiian basalt. Geochim Cosmochim Acta 68:4859–4876. https://doi.org/10.1016/j.gca.2004.06.005
Cismasu AC, Williams KH, Nico PS (2016) Iron and carbon dynamics during aging and reductive transformation of biogenic ferrihydrite. Environ Sci Technol 50:25–35. https://doi.org/10.1021/acs.est.5b03021
Coby AJ, Picardal F, Shelobolina E et al (2011) Repeated anaerobic microbial redox cycling of iron. Appl Environ Microbiol 77:6036–6042. https://doi.org/10.1128/AEM.00276-11
Coward EK, Thompson AT, Plante AF (2017) Iron-mediated mineralogical control of organic matter accumulation in tropical soils. Geoderma 306:206–216. https://doi.org/10.1016/j.geoderma.2017.07.026
Craine JM, Elmore AJ, Wang L et al (2015) Convergence of soil nitrogen isotopes across global climate gradients. Sci Rep 5:8280. https://doi.org/10.1038/srep08280
Demyan MS, Rasche F, Schulz E et al (2012) Use of specific peaks obtained by diffuse reflectance Fourier transform mid-infrared spectroscopy to study the composition of organic matter in a Haplic Chernozem. Eur J Soil Sci 63:189–199. https://doi.org/10.1111/j.1365-2389.2011.01420.x
Dubinsky EA, Silver WL, Firestone MK (2010) Tropical forest soil microbial communities couple iron and carbon biogeochemistry. Ecology 91:2604–2612. https://doi.org/10.1890/09-1365.1
Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422. https://doi.org/10.1890/1051-0761(2000)010[0412:CIRIBC]2.0.CO;2
Eusterhues K, Neidhardt J, Hädrich A et al (2014) Biodegradation of ferrihydrite-associated organic matter. Biogeochemistry 119:45–50. https://doi.org/10.1007/s10533-013-9943-0
Filimonova S, Kaufhold S, Wagner FE et al (2016) The role of allophane nano-structure and Fe oxide speciation for hosting soil organic matter in an allophanic Andosol. Geochim Cosmochim Acta 180:284–302. https://doi.org/10.1016/j.gca.2016.02.033
Fimmen RL, Richter D, Vasudevan D et al (2008) Rhizogenic Fe–C redox cycling: a hypothetical biogeochemical mechanism that drives crustal weathering in upland soils. Biogeochemistry 87:127–141
Fissore C, Dalzell BJ, Berhe AA et al (2017) Influence of topography on soil organic carbon dynamics in a Southern California grassland. Catena 149(Part 1):140–149. https://doi.org/10.1016/j.catena.2016.09.016
Ginn B, Meile C, Wilmoth J et al (2017) Rapid iron reduction rates are stimulated by high-amplitude redox fluctuations in a tropical forest soil. Environ Sci Technol 51:3250–3259. https://doi.org/10.1021/acs.est.6b05709
Gu B, Schmitt J, Chen Z et al (1994) Adsorption and desorption of natural organic matter on iron oxide: mechanisms and models. Environ Sci Technol 28:38–46
Hagedorn F, Kaiser K, Feyen H, Schleppi P (2000) Effects of redox conditions and flow processes on the mobility of dissolved organic carbon and nitrogen in a forest soil. J Environ Qual 29:288–297. https://doi.org/10.2134/jeq2000.00472425002900010036x
Hall SJ, Silver WL (2015) Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest. Biogeochemistry 125:149–165. https://doi.org/10.1007/s10533-015-0120-5
Hall SJ, McDowell WH, Silver WL (2013) When wet gets wetter: decoupling of moisture, redox biogeochemistry, and greenhouse gas fluxes in a humid tropical forest soil. Ecosystems 16:576–589. https://doi.org/10.1007/s10021-012-9631-2
Hall SJ, McNicol G, Natake T, Silver WL (2015) Large fluxes and rapid turnover of mineral-associated carbon across topographic gradients in a humid tropical forest: insights from paired 14C analysis. Biogeosciences 12:2471–2487. https://doi.org/10.5194/bg-12-2471-2015
Hall SJ, Silver WL, Timokhin VI, Hammel KE (2016) Iron addition to soil specifically stabilized lignin. Soil Biol Biochem 98:95–98. https://doi.org/10.1016/j.soilbio.2016.04.010
Herold N, Schöning I, Michalzik B et al (2014) Controls on soil carbon storage and turnover in German landscapes. Biogeochemistry 119:435–451. https://doi.org/10.1007/s10533-014-9978-x
Huang W, Hall SJ (2017) Elevated moisture stimulates carbon loss from mineral soils by releasing protected organic matter. Nat Commun 8:1774. https://doi.org/10.1038/s41467-017-01998-z
Kaiser K (2003) Sorption of natural organic matter fractions to goethite (α-FeOOH): effect of chemical composition as revealed by liquid-state 13C NMR and wet-chemical analysis. Org Geochem 34:1569–1579. https://doi.org/10.1016/S0146-6380(03)00120-7
Kaiser M, Ellerbrock RH, Wulf M et al (2012) The influence of mineral characteristics on organic matter content, composition, and stability of topsoils under long-term arable and forest land use. J Geophys Res Biogeosciences 117:G02018. https://doi.org/10.1029/2011JG001712
Kaiser M, Zederer DP, Ellerbrock RH et al (2016) Effects of mineral characteristics on content, composition, and stability of organic matter fractions separated from seven forest topsoils of different pedogenesis. Geoderma 263:1–7. https://doi.org/10.1016/j.geoderma.2015.08.029
Keiluweit M, Bougoure JJ, Zeglin LH et al (2012) Nano-scale investigation of the association of microbial nitrogen residues with iron (hydr)oxides in a forest soil O-horizon. Geochim Cosmochim Acta 95:213–226. https://doi.org/10.1016/j.gca.2012.07.001
Keiluweit M, Bougoure JJ, Nico PS et al (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Change 5:588–595. https://doi.org/10.1038/nclimate2580
Khomo L, Trumbore S, Bern CR, Chadwick OA (2017) Timescales of carbon turnover in soils with mixed crystalline mineralogies. Soil 3:17–30. https://doi.org/10.5194/soil-3-17-2017
Kleber M, Eusterhues K, Keiluweit M et al (2015) Mineral–organic associations: formation, properties, and relevance in soil environments. Adv Agron 130:1–140
Kögel-Knabner I, Guggenberger G, Kleber M et al (2008) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171:61–82. https://doi.org/10.1002/jpln.200700048
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 Change Biol 18:2594–2605. https://doi.org/10.1111/j.1365-2486.2012.02681.x
Larsen MC, Torres-Sánchez AJ, Concepción IM (1999) Slopewash, surface runoff and fine-litter transport in forest and landslide scars in humid-tropical steeplands, luquillo experimental forest, Puerto Rico. Earth Surf Process Landf 24:481–502. https://doi.org/10.1002/(SICI)1096-9837(199906)24:6<481::AID-ESP967>3.0.CO;2-G
Liu X, Eusterhues K, Thieme J et al (2013) STXM and NanoSIMS Investigations on EPS fractions before and after adsorption to goethite. Environ Sci Technol 47:3158–3166. https://doi.org/10.1021/es3039505
Loeppert R, Inskeep W (1996) Iron. In: Sparks D (ed) Methods of soil analysis, part 3—chemical methods. Soil Science Society of America, Madison, pp 639–664
Marin-Spiotta E, Swanston CW, Torn MS et al (2008) Chemical and mineral control of soil carbon turnover in abandoned tropical pastures. Geoderma 143:49–62. https://doi.org/10.1016/j.geoderma.2007.10.001
Masiello CA, Chadwick OA, Southon J et al (2004) Weathering controls on mechanisms of carbon storage in grassland soils. Glob Biogeochem Cycles 18:GB4023. https://doi.org/10.1029/2004gb002219
Mikutta R, Schaumann GE, Gildemeister D et al (2009) Biogeochemistry of mineral–organic associations across a long-term mineralogical soil gradient (0.3–4100 kyr), Hawaiian Islands. Geochim Cosmochim Acta 73:2034–2060. https://doi.org/10.1016/j.gca.2008.12.028
Pan W, Kan J, Inamdar S et al (2016) Dissimilatory microbial iron reduction release DOC (dissolved organic carbon) from carbon-ferrihydrite association. Soil Biol Biochem 103:232–240. https://doi.org/10.1016/j.soilbio.2016.08.026
Parikh SJ, Goyne KW, Margenot AJ et al (2014) Soil chemical insights provided through vibrational spectroscopy. Adv Agron 126:1–148
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Riedel T, Zak D, Biester H, Dittmar T (2013) Iron traps terrestrially derived dissolved organic matter at redox interfaces. Proc Natl Acad Sci USA 110:10101–10105. https://doi.org/10.1073/pnas.1221487110
Ryals R, Kaiser M, Torn MS et al (2014) Impacts of organic matter amendments on carbon and nitrogen dynamics in grassland soils. Soil Biol Biochem 68:52–61. https://doi.org/10.1016/j.soilbio.2013.09.011
Scatena FN, Lugo AE (1995) Geomorphology, disturbance, and the soil and vegetation of two subtropical wet steepland watersheds of Puerto Rico. Geomorphology 13:199–213. https://doi.org/10.1016/0169-555X(95)00021-V
Schulz M, Stonestrom D, Lawrence C et al (2016) Structured heterogeneity in a marine terrace chronosequence: upland mottling. Vadose Zone J. https://doi.org/10.2136/vzj2015.07.0102
Silver WL, Lugo AE, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–328. https://doi.org/10.1023/A:1006034126698
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
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
Swanston CW, Torn MS, Hanson PJ et al (2005) Initial characterization of processes of soil carbon stabilization using forest stand-level radiocarbon enrichment. Geoderma 128:52–62. https://doi.org/10.1016/j.geoderma.2004.12.015
Teh YA, Silver WL, Scatena FN (2009) A decade of belowground reorganization following multiple disturbances in a subtropical wet forest. Plant Soil 323:197–212. https://doi.org/10.1007/s11104-009-9926-z
Thompson A, Chadwick OA, Boman S, Chorover J (2006) Colloid mobilization during soil iron redox oscillations. Environ Sci Technol 40:5743–5749. https://doi.org/10.1021/es061203b
Thompson A, Rancourt DG, Chadwick OA, Chorover J (2011) Iron solid-phase differentiation along a redox gradient in basaltic soils. Geochim Cosmochim Acta 75:119–133. https://doi.org/10.1016/j.gca.2010.10.005
Torn MS, Trumbore SE, Chadwick OA et al (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173. https://doi.org/10.1038/38260
Veum KS, Goyne KW, Kremer RJ et al (2014) Biological indicators of soil quality and soil organic matter characteristics in an agricultural management continuum. Biogeochemistry 117:81–99. https://doi.org/10.1007/s10533-013-9868-7
Wagai E, Mayer L (2007) Sorptive stabilization of organic matter in soils by hydrous iron oxides. Geochim Cosmochim Acta 71:25–35. https://doi.org/10.1016/j.gca.2006.08.047
Wang Y, Wang H, He J-S, Feng X (2017) Iron-mediated soil carbon response to water-table decline in an alpine wetland. Nat Commun 8:15972. https://doi.org/10.1038/ncomms15972
Xiao J, He X, Hao J et al (2016) New strategies for submicron characterization the carbon binding of reactive minerals in long-term contrasting fertilized soils: implications for soil carbon storage. Biogeosciences 13:3607–3618. https://doi.org/10.5194/bg-13-3607-2016
Yang WH, Liptzin D (2015) High potential for iron reduction in upland soils. Ecology 96:2015–2020. https://doi.org/10.1890/14-2097.1
Zhao Q, Poulson SR, Obrist D et al (2016) Iron-bound organic carbon in forest soils: quantification and characterization. Biogeosciences 13:4777–4788. https://doi.org/10.5194/bg-13-4777-2016
Acknowledgements
Data from this study will be available from the CZO data portal (http://criticalzone.org/luquillo/data/). SJH gratefully acknowledges mentorship by Whendee Silver in previous work related to this study. We thank two anonymous reviewers for their constructive comments, Michael Kaiser for helpful feedback on DRIFTS interpretation, and Kimber Moreland and Nehru Mantripragada for performing DRIFTS and Mössbauer measurements, respectively. Funding was provided by NSF DEB-1457805 and the NSF Luquillo Critical Zone Observatory (NSF EAR-1331841). We acknowledge logistical support from the US Forest Service IITF.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Jan Mulder.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10533_2018_476_MOESM1_ESM.docx
Appendix: Details for Mössbauer analyses and modeled site populations for each measured sample, and DRIFTS data for each sample. Supplementary material 1 (DOCX 6727 kb)
Rights and permissions
About this article
Cite this article
Hall, S.J., Berhe, A.A. & Thompson, A. Order from disorder: do soil organic matter composition and turnover co-vary with iron phase crystallinity?. Biogeochemistry 140, 93–110 (2018). https://doi.org/10.1007/s10533-018-0476-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-018-0476-4