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Interaction of minerals, organic matter, and microorganisms during biogeochemical interface formation as shown by a series of artificial soil experiments

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Abstract

Our understanding of the interactions between minerals, organic matter, and microorganisms at so-called biogeochemical interfaces in soil is still hampered by the inherent complexity of these systems. Artificial soil maturation experiments can help to bridge a gap in complexity between simple abiotic sorption experiments and larger-scale field experiments. By controlling other soil-forming factors, the effect of a particular variable can be identified in a simplified system. Here, we review the findings of a series of artificial soil incubation experiments with the aim of revealing general trends and conclusions. The artificial soils were designed to determine the effect of mineral composition and charcoal presence on the development of abiotic and biotic soil properties during maturation. In particular, the development of soil aggregates, organic matter (OM) composition and turnover, sorption properties, and the establishment of microbial community composition and function were considered. The main objectives of the research were to determine (1) how surface properties and sorption of chemicals modify biogeochemical interfaces; (2) how much time is required to form aggregates from mixtures of pure minerals, OM, and a microbial inoculum; and (3) how the presence of different mineral and charcoal surfaces affects aggregation, OM turnover, and the development of microbial community composition.

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References

  • Amelung W, Miltner A, Zhang X, Zech W (2001) Fate of microbial residues during litter decomposition as affected by minerals. Soil Sci 166:598–606

    Article  CAS  Google Scholar 

  • Babin D, Ding GC, Pronk GJ, Heister K, Kögel-Knabner I, Smalla K (2013) Metal oxides, clay minerals and charcoal determine the composition of microbial communities in matured artificial soils and their response to phenanthrene. FEMS Microbiol Ecol 86:3–14

    Article  CAS  PubMed  Google Scholar 

  • Babin D, Vogel C, Zühlke S, Schloter M, Pronk GJ, Heister K, Spiteller M, Kögel-Knabner I, Smalla K (2014) Soil mineral composition matters: response of microbial communities to phenanthrene and plant litter addition in long-term matured artificial soils. PLoS One 9(9):e106865

    Article  PubMed  PubMed Central  Google Scholar 

  • Barré P, Fernandez-Ugalde O, Virto I, Velde B, Chenu C (2014) Impact of phyllosilicate mineralogy on organic carbon stabilization in soils: incomplete knowledge and exciting prospects. Geoderma 235–236:382–395

    Article  Google Scholar 

  • Bockheim JG, Gennadiyev AN (2009) The value of controlled experiments in studying soil-forming processes: a review. Geoderma 152:208–217

    Article  Google Scholar 

  • Brevik EC, Cerdà A, Mataix-Solera J, Pereg L, Quinton JN, Six J, Van Oost K (2015) The interdisciplinary nature of SOIL—ProQuest. Soil 1:117–129

    Article  Google Scholar 

  • Chorover J, Armistadi MK (2001) Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim Cosmochim Ac 65:95–109

    Article  CAS  Google Scholar 

  • Chorover J, Kretzschmar R, Garcia-Pichel F, Sparks DL (2007) Soil biogeochemical processes within the critical zone. Elements 3:321–326

    Article  CAS  Google Scholar 

  • Crawford JW, Deacon L, Grinev D, Harris JA, Ritz K, Singh BK, Young IA (2012) Microbial diversity affects self-organization of the soil-microbe system with consequences for function. J Roy Soc Interface 9:1301–1310

    Article  Google Scholar 

  • Dechesne A, Wang G, Gülez G, Or D, Smets BF (2010) Hydration-controlled bacterial motility and dispersal on surfaces. P Natl Aca dSci USA 107:14369–14372

    Article  CAS  Google Scholar 

  • Delmont TO, Francioli D, Jacquesson S, Laoudi S, Mathieu A, Nesme J, Ceccherini MT, Nannipieri P, Simonet P, Vogel TM (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol Fert Soils 50:1069–1076

    Article  CAS  Google Scholar 

  • Ding GC, Heuer H, Smalla K (2012) Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene: soil type specific and common responders. Front Microbiol 3:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding GC, Pronk GJ, Babin D, Heuer H, Heister K, Kögel-Knabner I, Smalla K (2013) Mineral composition and charcoal determine the bacterial community structure in artificial soils. FEMS MicrobiolEcol 86:15–25

    Article  CAS  Google Scholar 

  • Ditterich F, Poll C, Pronk GJ, Heister K, Chandran A, Rennert T, Kögel-Knabner I, Kandeler E (2016) Succession of soil microbial communities and enzyme activities in artificial soils. Pedobiologia 59:93–104

    Article  Google Scholar 

  • Dümig A, Smittenberg R, Kögel-Knabner I (2011) Concurrent evolution of organic and mineral components during initial soil development after retreat of the Damma glacier, Switzerland. Geoderma 163:83–94

    Article  Google Scholar 

  • Ellis RJ (2004) Artificial soil microcosms: a tool for studying microbial autecology under controlled conditions. J Microbiol Method 56:287–290

    Article  Google Scholar 

  • Epstein SS (2009) Microbial awakenings. Nature 457:1083

    Article  CAS  PubMed  Google Scholar 

  • Esperschütz J, Pérez-de-Mora A, Schreiner K, Welzl G, Buegger F, Zeyer J, Hagedorn F, Munch JC, Schloter M (2011) Microbial food web dynamics along a soil chronosequence of a glacier forefield. Biogeosci 8:3283–3294

    Article  Google Scholar 

  • Eusterhues K, Wagner FE, Häusler W, Hanzlik M, Knicker H, Totsche KU, Kögel-Knabner I, Schwertmann U (2008) Characterization of ferrihydrite-soil organic matter coprecipitates by X-ray diffraction and Mössbauer spectroscopy. Env Sci Technol 42:7891–7897

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Giebler J, Wick LY, Chatzinotas A, Harms H (2013) Alkane-degrading bacteria at the soil-litter interface: comparing isolates with T-RFLP-based community profiles. FEMS Microbiol Ecol 86:45–58

    Article  CAS  PubMed  Google Scholar 

  • Guenet B, Leloup J, Hartmann C, Barot S, Abbadie L (2011) A new protocol for an artificial soil to analyse soil microbiological processes. Appl Soil Ecol 48:243–246

    Article  Google Scholar 

  • Haberhauer G, Pfeiffer L, Gerzabek MH, Kirchmann H, Aquino AJA, Tunega D, Lischka H (2001) Response of sorption processes of MCPA to the amount and origin of organic matter in a long-term field experiment. Eur J Soil Sci 52:279–286

    Article  CAS  Google Scholar 

  • Hallsworth EG, Crawford DV (1965) Experimental pedology. Butterworths, London

    Google Scholar 

  • Heckman K, Grandy AS, Gao X, Keiluweit M, Wickings K, Carpenter K, Chorover J, Rasmussen C (2013a) Sorptive fractionation of organic matter and formation of organo-hydroxy-aluminum complexes during litter biodegradation in the presence of gibbsite. Geochim Cosmochim Ac 121:667–683

    Article  CAS  Google Scholar 

  • Heckman K, Vazquez-Ortega A, Gao X, Chorover J, Rasmussen C (2011) Changes in water extractable organic matter during incubation of forest floor material in the presence of quartz, goethite and gibbsite surfaces. Geochim Cosmochim Ac 75:4295–4309

    Article  CAS  Google Scholar 

  • Heckman K, Welty-Bernard A, Vazquez-Ortega A, Schwartz E, Chorover J, Rasmussen C (2013b) The influence of goethite and gibbsite on soluble nutrient dynamics and microbial community composition. Biogeochemistry 112:179–195

    Article  CAS  Google Scholar 

  • Heister K, Höschen C, Pronk GJ, Mueller CW, Kögel-Knabner I (2012) NanoSIMS as a tool for characterizing soil model compounds and organomineral associations in artificial soils. J Soils Sediment 12:35–47

    Article  CAS  Google Scholar 

  • Hemkemeyer M, Pronk GJ, Heister K, Kögel-Knabner I, Martens R, Tebbe CC (2014) Artificial soil studies reveal domain-specific preferences of microorganisms for the colonisation of different soil minerals and particle size fractions. FEMS Microbiol Ecol 90:770–782

    Article  CAS  PubMed  Google Scholar 

  • Huggett RJ (1998) Soil chronosequences, soil development, and soil evolution: a critical review. Catena 32:155–172

    Article  Google Scholar 

  • Jenny H (1941) Factors of soil formation: a system of quantitative pedology. McGraw-Hill, New York

    Google Scholar 

  • Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84

    Article  CAS  PubMed  Google Scholar 

  • Jozefaciuk G, Czachor H (2014) Impact of organic matter, iron oxides, alumina, silica and drying on mechanical and water stability of artificial soil aggregates. Assessment of new method to study water stability. Geoderma 221-222:1–10

    Article  CAS  Google Scholar 

  • Kaiser K, Guggenberger G, Zech W (1996) Sorption of DOM and DOM fractions to forest soils. Geoderma 74:281–303

    Article  Google Scholar 

  • Kaiser M, Kleber M, Myrold DD (2014) Influence of calcium carbonate and charcoal applications on organic matter storage in silt-sized aggregates formed during a microcosm experiment. Soil Sci Soc Am J 78:1624–1631

    Article  Google Scholar 

  • Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS (2015) Mineral–organic associations: formation, properties, and relevance in soil environments. Adv Agron 130:2–140

    Google Scholar 

  • Kunhi Mouvenchery Y (2013) Insight into physicochemical structure of soil organic matter by cation interaction and nanothermal properties. Dissertation, University Koblenz-Landau. http://kola.opus.hbz-nrw.de/frontdoor.php?source_opus=925&la=de

  • Lamparter A, Bachmann J, Woche SK, Goebel MO (2014) Biogeochemical interface formation: wettability affected by organic matter sorption and microbial activity. Vadose Zone J 13(7). doi:10.2136/vzj2013.10.0175

  • Leifeld J, Siebert S, Kögel-Knabner I (2001) Stabilization of composted organic matter after application to a humus-free sandy mining soil. J Environ Qual 30:602–607

    Article  CAS  PubMed  Google Scholar 

  • Leinweber P, Reuter G (1992) The influence of different organic fertilization practices on concentrations of organic carbon and total nitrogen in particle-size fractions during 34 years of a soil formation experiment in loamy marl. Biol Fert Soils 13:119–124

    Article  CAS  Google Scholar 

  • Macht F, Eusterhues K, Pronk GJ, Totsche KU (2011) Specific surface area of clay minerals: comparison between atomic force microscopy measurements and bulk-gas (N2) and -liquid (EGME) adsorption methods. Applied Clay Sci 53:20–26

    Article  CAS  Google Scholar 

  • Mikutta R, Schaumann G, Gildemeister D, Bonneville S, Kramer MG, Chorover J, Chadwick OA, Guggenberger G (2009) Biogeochemistry of mineral-organic associations across a long-term mineralogical soil gradient (0.3–4100 kyr), Hawaiian Islands. Geochim Cosmochim Ac 73:2034–2060

    Article  CAS  Google Scholar 

  • Mikutta R, Zang U, Chorover J, Haumaier L, Kalbitz K (2011) Stabilization of extracellular polymeric substances (Bacillus subtilis) by adsorption to and coprecipitation with Al forms. Geochim Cosmochim Ac 75:3135–3154

    Article  CAS  Google Scholar 

  • Miltner A, Zech W (1999) Microbial degradation and resynthesis of proteins during incubation of beech leaf litter in the presence of mineral phases. Biol Fert Soils 30:48–51

    Article  CAS  Google Scholar 

  • Muehl GJH, Ruehlmann J, Goebel MO, Bachmann J (2012) Application of confocal laser scanning microscopy (CLSM) to visualize the effect of porous media wettability on unsaturated pore water configuration. J Soils Sediments 12:75–85

    Article  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Nazir R, Semenov AV, Sarigul N, van Elsas JD (2013) Bacterial community establishment in native and non-native soils and the effect of fungal colonization. Microbiol Discovery 1:8 http://dx.doi.org/10.7243/2052-6180-1-8

    Article  Google Scholar 

  • Neumann D, Heuer A, Hemkemeyer M, Martens R, Tebbe CC (2013) Response of microbial communities to long-term fertilization depends on their microhabitat. FEMS Microbiol Ecol 86:71–84

    Article  CAS  PubMed  Google Scholar 

  • Oades J (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337

    Article  CAS  Google Scholar 

  • Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828

    Article  Google Scholar 

  • OECD (2004) Guideline for Testing Chemicals No. 222, Earthworm Reproduction Test. Paris

  • Or D, Smets BF, Wraith JM, Dechesne A, Friedman SP (2007) Physical constraints affecting bacterial habitats and activity in unsaturated porous media—a review. Adv Water Res 30:1505–1527

    Article  Google Scholar 

  • Pallud C, Kausch M, Fendorf S, Meile C (2009) Spatial patterns and modeling of reductive ferrihydrite transformation observed in artificial soil aggregates. Env Sci Technol 44:74–79

    Article  Google Scholar 

  • Pronk GJ (2011) Biogeochemical interfaces in natural and artificial soil systems: specific surface area, phenanthrene sorptive properties and formation of organo-mineral associations. Dissertation, Technische Universität München https://mediatum.ub.tum.de/?id=1081456.

  • Pronk GJ, Heister K, Ding GC, Smalla K, Kögel-Knabner I (2012) Development of biogeochemical interfaces in an artificial soil incubation experiment; aggregation and formation of organo-mineral associations. Geoderma 189–190:585–594

    Article  Google Scholar 

  • Pronk GJ, Heister K, Kögel-Knabner I (2013) Is turnover and development of organic matter controlled by mineral composition? Soil Biol Biochem 67:235–244

    Article  CAS  Google Scholar 

  • Pronk GJ, Heister K, Kögel-Knabner I (2015) Amino sugars reflect microbial residues as affected by clay mineral composition of artificial soils. Organic Geochem 83-84:109–113

    Article  CAS  Google Scholar 

  • Raynaud X, Nunan N (2014) Spatial ecology of bacteria at the microscale in soil. PLoS One 9:e87217

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruamps LS, Nunan N, Pouteau V, Leloup J, Raynaud X, Roy V, Chenu C (2013) Regulation of soil organic C mineralisation at the pore scale. FEMS Microbiol Ecol 86:26–35

    Article  CAS  PubMed  Google Scholar 

  • Saidy AR, Smernik RJ, Baldock JA, Kaiser K, Sanderman J, Macdonald LM (2012) Effects of clay mineralogy and hydrous iron oxides on labile organic carbon stabilisation. Geoderma 173–174:104–110

    Article  Google Scholar 

  • Schaaf W, Bens O, Fischer A, Gerke HH, Gerwin W, Gruenewald U, Holländer HM, Kögel-Knabner I, Mutz M, Schloter M, Schulin R, Veste M, Winter S, Huettl RF (2011) Patterns and processes of initial terrestrial-ecosystem development. J Plant Nutr Soil Sci 174:229–239

    Article  CAS  Google Scholar 

  • Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Frontiers Microbiol 3:1–11

    Article  Google Scholar 

  • Schnitzer M, Kodama H (1972) Differential thermal analysis of metal-fulvic acid salts and complexes. Geoderma 7:93–103

    Article  CAS  Google Scholar 

  • Schulz S, Giebler J, Chatzinotas A, Wick LY, Fetzer I, Welzl G, Harms H, Schloter M (2012) Plant litter and soil type drive abundance, activity and community structure of alkB harbouring microbes in different soil compartments. ISME J 6:1763–1774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schurig C, Smittenberg RH, Berger J, Kraft F, Woche SK, Goebel MO, Heipieper HJ, Miltner A, Kaestner M (2013) Microbial cell-envelope fragments and the formation of soil organic matter: a case study from a glacier forefield. Biogeochemistry 113:595–612

    Article  CAS  Google Scholar 

  • 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 Till Res 79:7–31

    Article  Google Scholar 

  • Steinbach A, Schulz S, Giebler J, Schulz S, Pronk GJ, Kögel-Knabner I, Harms H, Wick LY, Schloter M (2015) Clay minerals and metal oxides strongly influence the structure of alkane-degrading microbial communities during soil maturation. ISME J 9:1687–1691

    Article  CAS  PubMed  Google Scholar 

  • Sukul P, Lamshöft M, Zühlke S, Spiteller M (2013) Evaluation of sorption-desorption processes for metalaxyl in natural and artificial soils. J Environ Sci Heal B 48:431–441

    Article  CAS  Google Scholar 

  • Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163

    Article  CAS  Google Scholar 

  • Totsche KU, Rennert T, Gerzabek MH, Kögel-Knabner I, Smalla K, Spiteller M, Vogel HJ (2010) Biogeochemical interfaces in soil: the interdisciplinary challenge for soil science. J Plant Nutr Soil Sc 173:88–99

    Article  CAS  Google Scholar 

  • Treves DS, Xia B, Zhou J, Tiedje JM (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45:20–28

    Article  CAS  PubMed  Google Scholar 

  • Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E (2003) Functional diversity of the soil microbial community in primary succession along two glacier forelands in the Central Alps. Eur J Soil Sci 54:685–696

    Article  Google Scholar 

  • Vogel C, Babin D, Pronk GJ, Heister K, Smalla K, Kögel-Knabner I (2014) Establishment of macro-aggregates and organic matter turnover by microbial communities in long-term incubated artificial soils. Soil Biol Biochem 79:1–11

    Article  Google Scholar 

  • Vogel C, Heister K, Buegger F, Tanuwidjaja I, Haug S, Schloter M, Kögel-Knabner I (2015) Clay mineral composition modifies decomposition and sequestration of organic carbon and nitrogen in fine soil fractions. Biol Fert Soils 51:427–442

    Article  CAS  Google Scholar 

  • Vos M, Wolf AB, Jennings SJ, Kowalchuk GA (2013) Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol Rev 37:936–954

    Article  CAS  PubMed  Google Scholar 

  • Wagner S, Cattle SR, Scholten T (2007) Soil-aggregate formation as influenced by clay content and organic-matter amendment. J Plant Nutr Soil Sci 170:173–180

    Article  CAS  Google Scholar 

  • Waldner G, Friesl-Hanl W, Haberhauer G, Gerzabek MH (2012) Differences in sorption behavior of the herbicide 4-chloro-2-methylphenoxyacetic acid on artificial soils as a function of soil pre-aging. J Soils Sediments 12:1292–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei H, Guenet B, Vicca S, Nunan N, AbdElgawad H, Pouteau V, Shen W, Janssens IA (2014a) Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure. Soil Biol Biochem 71:1–12

    Article  CAS  Google Scholar 

  • Wei H, Guenet B, Vicca S, Nunan N, Asard H, AbdElgawad H, Shen W, Janssens IA (2014b) High clay content accelerates the decomposition of fresh organic matter in artificial soils. Soil Biol Biochem 77:100–108

    Article  CAS  Google Scholar 

  • Weigand H, Totsche KU (1998) Flow and reactivity effects on dissolved organic matter transport in soil columns. Soil Sci Soc Am J 62:1268–1274

    Article  CAS  Google Scholar 

  • Wolf AB, Vos M, de Boer W, Kowalchuk GA (2013) Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria. PLoS One 8:e83661

    Article  PubMed  PubMed Central  Google Scholar 

  • Young IM, Crawford JW (2004) Interactions and self-organization in the soil-microbe complex. Science 304:1634–1637

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Loynachan TE, Raich JW (2011) Artificial soils to assess temperature sensitivity of the decomposition of model organic compounds: effects of chemical recalcitrance and clay-mineral composition. Eur J Soil Sci 62:863–873

    Article  CAS  Google Scholar 

  • Zehetner F, Lair GJ, Gerzabek MH (2009) Rapid carbon accretion and organic matter pool stabilization in riverine floodplain soils. Global Biogeochem Cy 23:GB4004

    Article  Google Scholar 

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Acknowledgements

This project was carried out within the framework of the priority program 1315 “Biogeochemical Interfaces in Soil” funded by the German Research Foundation (DFG) in the project “Parent materials as major properties of the biogeochemical interface: integrative analysis” (KO1035/45-1). I.K.-K. and G.J.P. are grateful for the support from the Technical University of Munich–Institute for Advanced Study, funded by the German Excellence Initiative. We thank two anonymous reviewers for valuable comments on the manuscript.

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Correspondence to Geertje J. Pronk.

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M.S. and I.K.-K. contributed equally to the manuscript

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Pronk, G.J., Heister, K., Vogel, C. et al. Interaction of minerals, organic matter, and microorganisms during biogeochemical interface formation as shown by a series of artificial soil experiments. Biol Fertil Soils 53, 9–22 (2017). https://doi.org/10.1007/s00374-016-1161-1

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