Mineral composition and charcoal determine the bacterial community structure in artificial soils
Guo-Chun Ding
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorGeertje Johanna Pronk
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Institute for Advanced Study, Technische Universität München, Garching, Germany
Search for more papers by this authorDoreen Babin
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorHolger Heuer
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorKatja Heister
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Search for more papers by this authorIngrid Kögel-Knabner
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Institute for Advanced Study, Technische Universität München, Garching, Germany
Search for more papers by this authorCorresponding Author
Kornelia Smalla
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Correspondence: Kornelia Smalla, JKI, Messeweg 11-12, 38104 Braunschweig, Germany. Tel.: +49-531-2993814; fax: +49-531-2993006; e-mail: [email protected]Search for more papers by this authorGuo-Chun Ding
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorGeertje Johanna Pronk
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Institute for Advanced Study, Technische Universität München, Garching, Germany
Search for more papers by this authorDoreen Babin
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorHolger Heuer
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Search for more papers by this authorKatja Heister
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Search for more papers by this authorIngrid Kögel-Knabner
Lehrstuhl für Bodenkunde, Technische Universität München, Freising-Weihenstephan, Germany
Institute for Advanced Study, Technische Universität München, Garching, Germany
Search for more papers by this authorCorresponding Author
Kornelia Smalla
Julius Kühn-Institut (JKI), Federal Research Centre for Cultivated Plants, Braunschweig, Germany
Correspondence: Kornelia Smalla, JKI, Messeweg 11-12, 38104 Braunschweig, Germany. Tel.: +49-531-2993814; fax: +49-531-2993006; e-mail: [email protected]Search for more papers by this authorAbstract
To study the influence of the clay minerals montmorillonite (M) and illite (I), the metal oxides ferrihydrite (F) and aluminum hydroxide (A), and charcoal (C) on soil bacterial communities, seven artificial soils with identical texture provided by quartz (Q) were mixed with sterilized manure as organic carbon source before adding a microbial inoculant derived from a Cambisol. Bacterial communities established in artificial soils after 90 days of incubation were compared by DGGE analysis of bacterial and taxon-specific 16S rRNA gene amplicons. The bacterial community structure of charcoal-containing soils highly differed from the other soils at all taxonomic levels studied. Effects of montmorillonite and illite were observed for Bacteria and Betaproteobacteria, but not for Actinobacteria or Alphaproteobacteria. A weak influence of metal oxides on Betaproteobacteria was found. Barcoded pyrosequencing of 16S rRNA gene amplicons done for QM, QI, QIF, and QMC revealed a high bacterial diversity in the artificial soils. The composition of the artificial soils was different from the inoculant, and the structure of the bacterial communities established in QMC soil was most different from the other soils, suggesting that charcoal provided distinct microenvironments and biogeochemical interfaces formed. Several populations with discriminative relative abundance between artificial soils were identified.
Supporting Information
| Filename | Description |
|---|---|
| fem12070-sup-0001-FigureS1.tifimage/tif, 4.6 MB | Fig. S1. DGGE fingerprint of actinobacterial 16S rRNA gene amplicons (a) and the corresponding UPGMA clusters (b) for different artificial soils collected 90 days after incubation (Q, quartz sand; M, montmorillonite; I, illite; F, ferrihydrite; A, aluminum hydroxide; and C, charcoal). |
| fem12070-sup-0002-FigureS2.tifimage/tif, 2.8 MB | Fig. S2. DGGE fingerprint of alphaproteobacterial 16S rRNA gene amplicons (a) and the corresponding UPGMA clusters (b) for different artificial soils collected 90 days after incubation (Q, quartz sand; M, montmorillonite; I, illite; F, ferrihydrite; A, aluminum hydroxide; and C, charcoal). |
| fem12070-sup-0003-FigureS3.tifimage/tif, 4.7 MB | Fig. S3. DGGE fingerprint of betaproteobacterial 16S rRNA gene amplicons (a) and the corresponding UPGMA clusters (b) for different artificial soils collected 90 days after incubation (Q: quartz sand; M: montmorillonite; I: illite; F: ferrihydrite; A: aluminum hydroxide and C: charcoal). |
| fem12070-sup-0004-FigureS4.tifimage/tif, 3.3 MB | Fig. S4. DGGE fingerprint of bacterial 16S rRNA gene amplicons (a) and the corresponding UPGMA clusters (b) for different artificial soils collected 1, 9, and 31 days after incubation (Q, quartz sand; M, montmorillonite; I, illite; F, ferrihydrite; and C, charcoal). |
| fem12070-sup-0005-FigureS5.tifimage/tif, 164 KB | Fig. S5. UPGMA cluster analysis of bacterial community structure for four selected artificial soils based on Bray-Curtis dissimilarity using the relative abundance (%) of OTU (> 97% sequence similarity of 16S rRNA gene amplicon) as the species data. Number in brackets: number of sequences obtained for the sample. Numbers on node: Bootstrapping value for each node means the percent frequency of all samples under the node grouping exclusively together. (Q, quartz sand; M, montmorillonite; I, illite; F, ferrihydrite; and C, charcoal). |
| fem12070-sup-0006-FigureS6.tifimage/tif, 644.3 KB | Fig. S6. Plot of rarefaction curves for the four selected artificial soils with different composition (Q, quartz sand; M: montmorillonite; I, illite; F, ferrihydrite; C, charcoal; and ino, inoculant). |
| fem12070-sup-0007-TableS1.docxWord document, 13.5 KB | Table S1. Percent of different taxa detected for different artificial soil samples 90 days after incubation. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Ams DA, Fein JB, Dong HL & Maurice PA (2004) Experimental measurements of the adsorption of Bacillus subtilis and Pseudomonas mendocina onto Fe-oxyhydroxide-coated and uncoated quartz grains. Geom J 21: 511–519.
- Ball PN, MacKenzie MD, DeLuca TH & Holben WE (2010) Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry Montane forest soils. J Environ Qual 39: 1243–1253.
- Bell MJ & Worrall F (2011) Charcoal addition to soils in NE England: a carbon sink with environmental co-benefits? Sci Total Environ 409: 1704–1714.
- Bissett A, Richardson AE, Baker G & Thrall PH (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51: 66–78.
- Calderon FJ, Jackson LE, Scow KM & Rolston DE (2001) Short-term dynamics of nitrogen, microbial activity, and phospholipid fatty acids after tillage. Soil Sci Soc Am J 65: 118–126.
- Carson JK, Campbell L, Rooney D, Clipson N & Gleeson DB (2009) Minerals in soil select distinct bacterial communities in their microhabitats. FEMS Microbiol Ecol 67: 381–388.
- Carson JK, Gonzalez-Quinones V, Murphy DV, Hinz C, Shaw JA & Gleeson DB (2010) Low pore connectivity increases bacterial diversity in soil. Appl Environ Microbiol 76: 3936–3942.
- Cheshire MV, Dumat C, Fraser AR, Hillier S & Staunton S (2000) The interaction between soil organic matter and soil clay minerals by selective removal and controlled addition of organic matter. Eur J Soil Sci 51: 497–509.
- Child R, Miller CD, Liang Y, Sims RC & Anderson AJ (2007) Pyrene mineralization by Mycobacterium sp strain KMS in a Barley rhizosphere. J Environ Qual 36: 1260–1265.
- Curtis TP, Sloan WT & Scannell JW (2002) Estimating prokaryotic diversity and its limits. P Natl Acad Sci USA 99: 10494–10499.
- Denef K & Six J (2005) Clay mineralogy determines the importance of biological versus abiotic processes for macroaggregate formation and stabilization. Euro J Soil Sci 56: 469–479.
- Denef K, Six J, Merckx R & Paustian K (2002) Short-term effects of biological and physical forces on aggregate formation in soils with different clay mineralogy. Plant Soil 246: 185–200.
- 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.
- Elad Y, David DR, Harel YM, Borenshtein M, Ben Kalifa H, Silber A & Graber ER (2010) Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 100: 913–921.
- Fierer N & Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103: 626–631.
- Fierer N, Bradford MA & Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88: 1354–1364.
- Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA & Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6: 1007–1017.
- Filip Z (1973) Clay minerals as a factor influencing biochemical activity of soil microorganisms. Folia Microbiol 18: 56–74.
- Gans J, Wolinsky M & Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309: 1387–1390.
- Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonça-Hagler L & Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232: 167–180.
- Gomes NC, Kosheleva IA, Abraham WR & Smalla K (2005) Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol Ecol 54: 21–33.
- Heuer H, Krsek M, Baker P, Smalla K & Wellington EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233–3241.
- Heuer H, Wieland J, Schönwälder A, Gomes NCM & Smalla K (2001) Bacterial community profiling using DGGE or TGGE analysis. Environmental Molecular Microbiology: Protocols and Applications ( PA Rochelle, ed), pp. 177–190. Horizon Scientific Press, Wymondham, UK.
- Hong SH, Bunge J, Jeon SO & Epstein SS (2006) Predicting microbial species richness. P Natl Acad Sci USA 103: 117–122.
- Hothorn T, Bretz F & Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50: 346–363.
- Huang PM, Wang MK & Chiu CY (2005) Soil mineral-organic matter-microbe interactions: impacts on biogeochemical processes and biodiversity in soils. Pedobiologia 49: 609–635.
- Johnsen AR, Wick LY & Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133: 71–84.
- Köberl M, Müller H, Ramadan EM & Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS ONE 6: e24452.
- Kramer S & Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32: 179–188.
- Lauber CL, Hamady M, Knight R & Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75: 5111–5120.
- Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC & Crowley D (2011) Biochar effects on soil biota – a review. Soil Biol Biochem 43: 1812–1836.
- Liu YJ, Zaprasis A, Liu SJ, Drake HL & Horn MA (2010) The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. ISME J 5: 473–485.
- Macht F, Eusterhues K, Pronk GJ & Totsche KU (2011) Specific surface area of clay minerals: comparison between atomic force microscopy measurements and bulk-gas (N-2) and -liquid (EGME) adsorption methods. Appl Clay Sci 53: 20–26.
- Mills AL, Herman JS, Hornberger GM & Dejesus TH (1994) Effect of solution ionic strength and iron coatings on mineral grains on the sorption of bacterial cells to quartz sand. Appl Environ Microbiol 60: 3300–3306.
- Morales SE, Cosart TF, Johnson JV & Holben WE (2009) Extensive phylogenetic analysis of a soil bacterial community illustrates extreme taxon evenness and the effects of amplicon length, degree of coverage, and DNA fractionation on classification and ecological parameters. Appl Environ Microbiol 75: 668–675.
- Mummey DL & Stahl PD (2004) Analysis of soil whole- and inner-microaggregate bacterial communities. Microb Ecol 48: 41–50.
- Nacke H, Thürmer A, Wollherr A et al. (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in german forest and grassland soils. PLoS ONE 6: e17000.
- Nechitaylo TY, Yakimov MM, Godinho M et al. (2010) Effect of the earthworms Lumbricus terrestris and Aporrectodea caliginosa on bacterial diversity in soil. Microb Ecol 59: 574–587.
- Peng JJ, Cai C, Qiao M, Li H & Zhu YG (2010) Dynamic changes in functional gene copy numbers and microbial communities during degradation of pyrene in soils. Environ Pollut 158: 2872–2879.
- Pronk GJ, Heister K, Ding G-C, 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.
- Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J & Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188–7196.
- Rhodes AH, McAllister LE, Chen R & Semple KT (2010) Impact of activated charcoal on the mineralisation of 14C-phenanthrene in soils. Chemosphere 79: 463–469.
- Rong X, Huang Q, He X, Chen H, Cai P & Liang W (2008) Interaction of Pseudomonas putida with kaolinite and montmorillonite: a combination study by equilibrium adsorption, ITC, SEM and FTIR. Colloids Surf B 64: 49–55.
- Rovira P, Duguy B & Vallejo VR (2009) Black carbon in wildfire-affected shrubland Mediterranean soils. J Plant Nutr Soil Sci 172: 43–52.
- Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537–7541.
- Sohi SP, Krull E, Lopez-Capel E & Bol R (2010) A review of biochar and its use and function in soil. Adv Agron 105: 47–82.
- Stotzky G (1986) Influence of soil mineral colloids on metabolic processes, growth, adhesion and ecology of microbes and viruses. Interactions of Soil Minerals with Natural Organics and Microbes: Special Publication No 17 ( PM Huang & M Schmitzer, eds), pp. 305–428. Soil Science Society of America, Madison, WI.
- Takai K & Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66: 5066–5072.
- 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 Sci 173: 88–99.
- Tunega D, Haberkauer G, Gerzabek MH & Lischka H (2004) Sorption of phenoxyacetic acid herbicides on the kaolinite mineral surface – an ab initio molecular dynamics simulation. Soil Sci 169: 44–54.
- Waldrop MP & Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol 52: 470–479.
- Wang Q, Garrity GM, Tiedje JM & Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261–5267.
- Yee N, Fein JB & Daughney CJ (2000) Experimental study of the pH, ionic strength, and reversibility behavior of bacteria-mineral adsorption. Geochim Cosmochim Acta 64: 609–617.
- Young IM & Crawford JW (2004) Interactions and self-organization in the soil-microbe complex. Science 304: 1634–1637.
- Yrjala K, Keskinen AK, Akerman ML, Fortelius C & Sipila TP (2010) The rhizosphere and PAH amendment mediate impacts on functional and structural bacterial diversity in sandy peat soil. Environ Pollut 158: 1680–1688.
- Zak DR, Holmes WE, White DC, Peacock AD & Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84: 2042–2050.
