Abstract
Biopores are hotspots of nutrient mobilisation and shortcuts for carbon (C) into subsoils. C processing relies on microbial community composition, which remains unexplored in subsoil biopores. Phospholipid fatty acids (PLFAs; markers for living microbial groups) and amino sugars (microbial necromass markers) were extracted from two subsoil depths (45–75 cm ; 75–105 cm) and three biopore types: (I) drilosphere of Lumbricus terrestris L., (II) 2-year-old root biopores and (III) 1.5-year-old root biopores plus six 6 months of L. terrestris activities. Biopore C contents were at least 2.5 times higher than in bulk soil, causing 26–35 times higher Σ PLFAs g-1 soil. The highest Σ PLFAs were found in both earthworm biopore types; thus, the highest soil organic matter and nutrient turnover were assumed. Σ PLFAs was 33% lower in root pores than in earthworm pores. The treatment affected the microbial community composition more strongly than soil depth, hinting to similar C quality in biopores: Gram-positives including actinobacteria were more abundant in root pores than in earthworm pores, probably due to lower C bioavailability in the former. Both earthworm pore types featured fresh litter input, promoting growth of Gram-negatives and fungi. Earthworms in root pores shifted the composition of the microbial community heavily and turned root pores into earthworm pores within 6 months. Only recent communities were affected and they reflect a strong heterogeneity of microbial activity and functions in subsoil hotspots, whereas biopore-specific necromass accumulation from different microbial groups was absent.
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References
Aira M, McNamara N, Piearce T, Domínguez J (2009) Microbial communities of Lumbricus terrestris L. middens: structure, activity, and changes through time in relation to earthworm presence. J Soils Sediments 9:54–61
Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Assessment methods for soil carbon; [papers from the International Workshop on “Assessment Methods for Soil C Pools”, held at The Ohio State University, Columbus Ohio, in November 1998]. Lewis, Boca Raton, pp 233–272
Amelung W (2003) Nitrogen biomarkers and their fate in soil. J Plant Nutr Soil Sci 166:677–686
Andriuzzi WS, Bolger T, Schmidt O (2013) The drilosphere concept. Fine-scale incorporation of surface residue-derived N and C around natural Lumbricus terrestris burrows. Soil Biol Biochem 64:136–138
Apostel C, Dippold MA, Glaser B, Kuzyakov Y (2013) Biochemical pathways of amino acids in soil: assessment by position-specific labeling and 13C-PLFA analysis. Soil Biol Biochem 67:31–40
Athmann M, Kautz T, Pude R, Köpke U (2013) Root growth in biopores—evaluation with in situ endoscopy. Plant Soil 371:179–190
Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963
Bach EM, Baer SG, Meyer CK, Six J (2010) Soil texture affects soil microbial and structural recovery during grassland restoration. Soil 42:2182–2191
Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Special issue: knowledge gaps in soil C and N interactions. Soil Biol Biochem 43:718–725
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Blume E, Bischoff M, Reichert JM, Moorman T, Konopka A, Turco RF (2002) Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season. Appl Soil Ecol 20:171–181
Bouché MB (1975) Action de la faune sur les états de la matière organique dans les écosystèmes. In: Gilbertus K, Reisinger O, Mourey A, Cancela da Fonseca JA (eds) Biodegradation et Humification. Pierron Editeur, Sarreguemines, pp 157–168
Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232
Brown GG (1995) How do earthworms affect microfloral and faunal community diversity? Springer, Dordrecht
Butt KR, Lowe CN (2007) A viable technique for tagging earthworms using visible implant elastomer. Appl Soil Ecol 35:454–457
Chen M-M, Zhu Y-G, Su Y-H, Chen B-D, Fu B-J, Marschner P (2007) Effects of soil moisture and plant interactions on the soil microbial community structure. Eur J Soil Biol 43:31–38
Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536
Devliegher W, Verstraete W (1997) Microorganisms and soil physico-chemical conditions in the drilosphere of Lumbricus terrestris. Soil Biol Biochem 29:1721–1729
Don A, Steinberg B, Schöning I, Pritsch K, Joschko M, Gleixner G, Schulze E-D (2008) Organic carbon sequestration in earthworm burrows. Soil Biol Biochem 40:1803–1812
Dorodnikov M, Fangmeier A, Kuzyakov Y (2007) Thermal stability of soil organic matter pools and their δ13C values after C3–C4 vegetation change. Soil Biol Biochem 39:1173–1180
Drenovsky RE, Elliott GN, Graham KJ, Scow KM (2004) Comparison of phospholipid fatty acid (PLFA) and total soil fatty acid methyl esters (TSFAME) for characterizing soil microbial communities. Soil Biol Biochem 36:1793–1800
Dziejowski JE, Rimmer A, Steenhuis TS (1997) Preferential movement of oxygen in soils? Soil Sci Soc Am J 61:1607–1610
Ehlers W, Köpke U, Hesse F, Böhm W (1983) Penetration resistance and root growth of oats in tilled and untilled loess soil. Soil Till Res 3:261–275
Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39:2111–2118
Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter. A question of microbial competition? Soil Biol Biochem 35:837–843
Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280
Franzmann PD, Zappia LR, Patterson BM, Rayner JL, Davis GB (1998) Mineralisation of low concentrations of organic compounds and microbial biomass in surface and vadose zone soils from the Swan Coastal Plain, Western Australia. Aust J Soil Res 36:921–940
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65
Frostegård Å, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14:151–163
Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625
Glaser B, Gross S (2005) Compound-specific delta13C analysis of individual amino sugars—a tool to quantify timing and amount of soil microbial residue stabilization. Rapid Commun Mass Spectrom 19:1409–1416
Glaser B, Turrión M-B, Alef K (2004) Amino sugars and muramic acid—biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407
Gliński J, Lipiec J (1990) Soil physical conditions and plant roots. CRC Press, Boca Raton
Görres JH, Savin MC, Amador JA (1997) Dynamics of carbon and nitrogen mineralization, microbial biomass, and nematode abundance within and outside the burrow walls of anecic earthworms (Lumbricus terrestris). Soil Sci 162:666–671
Graff O (1967) Über die Verlagerung von Nährelementen in den Unterboden durch Regenwurmtätigkeit. Landw Forsch 20:117–127
Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1998) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153
Guenet B, Lenhart K, Leloup J, Giusti-Miller S, Pouteau V, Mora P, Nunan N, Abbadie L (2012) The impact of long-term CO2 enrichment and moisture levels on soil microbial community structure and enzyme activities. Geoderma 170:331–336
Gunina A, Kuzyakov Y (2014) Pathways of litter C by formation of aggregates and SOM density fractions: implications from 13C natural abundance. Soil Biol Biochem 71:95–104
Gunina A, Dippold MA, Glaser B, Kuzyakov Y (2014) Fate of low molecular weight organic substances in an arable soil: from microbial uptake to utilisation and stabilisation. Soil Biol Biochem 77:304–313
Hafner S, Kuzyakov Y (2016) Carbon input and partitioning in subsoil by chicory and alfalfa. Plant Soil 406:29–42
Hammer Ø, Harper D, Ryan P (2001) PAST. Palaeontol Electron 4:9
Han E, Kautz T, Perkons U, Uteau D, Peth S, Huang N, Horn R, Köpke U (2015) Root growth dynamics inside and outside of soil biopores as affected by crop sequence determined with the profile wall method. Biol Fertil Soils 51:847–856
Harwood JL, Russell NJ (1984) Lipids in plants and microbes. Springer, Dordrecht
Herrmann AM, Coucheney E, Nunan N (2014) Isothermal microcalorimetry provides new insight into terrestrial carbon cycling. Environ Sci Technol 48:4344–4352
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
Hirth JR, McKenzie BM, Tisdall JM (2005) Ability of seedling roots of Lolium perenne L. to penetrate soil from artificial biopores is modified by soil bulk density, biopore angle and biopore relief. Plant Soil 272:327–336
Hoang DTT, Pausch J, Razavi BS, Kuzyakova I, Banfield CC, Kuzyakov Y (2016) Hotspots of microbial activity induced by earthworm burrows, old root channels, and their combination in subsoil. Biol Fertil Soils 52:1105–1119
Hueso S, García C, Hernández T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50:167–173
IUSS Working Group WRB (2008) World reference base for soil resources (2006). Ein Rahmen für internationale Klassifikation, Korrelation und Kommunikation. BGR, Hannover
Jastrow J, Amonette J, Bailey V (2007) Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Clim Chang 80:5–23
Jégou D, Cluzeau D, Balesdent J, Tréhen P (1998) Effects of four ecological categories of earthworms on carbon transfer in soil. Appl Soil Ecol 9:249–255
Jégou D, Cluzeau D, Hallaire V, Balesdent J, Tréhen P (2000) Burrowing activity of the earthworms Lumbricus terrestris and Aporrectodea giardi and consequences on C transfers in soil. Eur J Soil Biol 36:27–34
Jégou D, Schrader S, Diestel H, Cluzeau D (2001) Morphological, physical and biochemical characteristics of burrow walls formed by earthworms. Appl Soil Ecol 17:165–174
Kautz T (2015) Research on subsoil biopores and their functions in organically managed soils: a review. Renew Agric Food Syst 30:318–327
Kautz T, Amelung W, Ewert F, Gaiser T, Horn R, Jahn R, Javaux M, Kemna A, Kuzyakov Y, Munch J-C, Pätzold S, Peth S, Scherer HW, Schloter M, Schneider H, Vanderborght J, Vetterlein D, Walter A, Wiesenberg GL, Köpke U (2013) Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biol Biochem 57:1003–1022
Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Phil Trans R Soc B 367:1589–1597
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 171:61–82
Kramer C, Gleixner G (2008) Soil organic matter in soil depth profiles. Distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem 40:425–433
Kuhlmann H, Baumgärtel G (1991) Potential importance of the subsoil for the P and Mg nutrition of wheat. Plant Soil 137:259–266
Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:382–396
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199
Lal R, Akinremi OO (1983) Physical properties of earthworm casts and surface soil as influenced my management. Soil Sci 135:114–122
Lauer F, Kösters R, Du Preez CC, Amelung W (2011) Microbial residues as indicators of soil restoration in South African secondary pastures. Soil Biol Biochem 43:787–794
Lee KE (1985) Earthworms. Their ecology and relationships with soils and land use. Academic Press, Sydney
Lipiec J, Brzezińska M, Turski M, Szarlip P, Frąc M (2015) Wettability and biogeochemical properties of the drilosphere and casts of endogeic earthworms in pear orchard. Soil Till Res 145:55–61
Lorenz K, Lal R (2007) The depth distribution of soil organic carbon in relation to land use and management and the potential of carbon sequestration in subsoil horizons. In: Sparks DL (ed) Advances in agronomy. Academic Press, San Diego, pp 35–66
Lozán JL, Kausch H (1998) Angewandte Statistik für Naturwissenschaftler. Parey Buchverlag, Singhofen
Lundquist E, Scow K, Jackson L, Uesugi S, Johnson C (1999) Rapid response of soil microbial communities from conventional, low input, and organic farming systems to a wet/dry cycle. Soil Biol Biochem 31:1661–1675
McCarthy AJ, Williams ST (1992) Actinomycetes as agents of biodegradation in the environment—a review. Gene 115:189–192
Millar WN, Casida LE (1970) Evidence for muramic acid in soil. Can J Microbiol 16:299–304
Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55
Moll J, Goldmann K, Kramer S, Hempel S, Kandeler E, Marhan S, Ruess L, Krüger D, Buscot F (2015) Resource type and availability regulate fungal communities along arable soil profiles. Microb Ecol 70:390–399
Nakamoto T (2000) The distribution of wheat and maize roots as influenced by biopores in a subsoil of the Kanto loam type. Plant Prod Sci 3:140–144
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Science 54:655–670
Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310
Parkin TB, Berry EC (1999) Microbial nitrogen transformations in earthworm burrows. Soil Biol Biochem 31:1765–1771
Parsons JW (1981) Chemistry and distribution of amino sugars in soils and soil organisms. In: Paul EA, Ladd JN (Eds) Soil Biochemistry, New York, NY, USA, pp 197–227
Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610
Perkons U, Kautz T, Uteau D, Peth S, Geier V, Thomas K, Lütke Holz K, Athmann M, Pude R, Köpke U (2014) Root-length densities of various annual crops following crops with contrasting root systems. Soil Till Res 137:50–57
Ponge J-F (2015) The soil as an ecosystem. Biol Fertil Soils 51:645–648
Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388
Rousk J, Brookes PC, Bååth E (2010) The microbial PLFA composition as affected by pH in an arable soil. Soil Biol Biochem 42:516–520
Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant Soil 338:143–158
Salome C, Nunan N, Pouteau V, Lerch TZ, Chenu C (2010) Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob Change Biol 16:416–426
Sampedro L, Whalen JK (2007) Changes in the fatty acid profiles through the digestive tract of the earthworm Lumbricus terrestris L. Appl Soil Ecol 35:226–236
Sampedro L, Jeannotte R, Whalen JK (2006) Trophic transfer of fatty acids from gut microbiota to the earthworm Lumbricus terrestris L. Soil Biol Biochem 38:2188–2198
Sanaullah M, Chabbi A, Leifeld J, Bardoux G, Billou D, Rumpel C (2011) Decomposition and stabilization of root litter in top-and subsoil horizons: what is the difference? Plant Soil 338:127–141
Sanaullah M, Chabbi A, Maron P-A, Baumann K, Tardy V, Blagodatskaya E, Kuzyakov Y, Rumpel C (2016) How do microbial communities in top-and subsoil respond to root litter addition under field conditions? Soil Biol Biochem 103:28–38
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
Schrader S, Rogasik H, Onasch I, Jégou D (2007) Assessment of soil structural differentiation around earthworm burrows by means of X-ray computed tomography and scanning electron microscopy. Geoderma 137:378–387
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–568
Sleutel S, Bouckaert L, Buchan D, van Loo D, Cornelis WM, Sanga HG (2012) Manipulation of the soil pore and microbial community structure in soil mesocosm incubation studies. Soil Biol Biochem 45:40–48
Stewart JB, Moran CJ, Wood JT (1999) Macropore sheath: quantification of plant root and soil macropore association. Plant Soil 211:59–67
Stromberger ME, Keith AM, Schmidt O (2012) Distinct microbial and faunal communities and translocated carbon in Lumbricus terrestris drilospheres. Soil Biol Biochem 46:155–162
Struecker J, Joergensen RG (2015) Microorganisms and their substrate utilization patterns in topsoil and subsoil layers of two silt loams, differing in soil organic C accumulation due to colluvial processes. Soil Biol Biochem 91:310–317
Tiunov AV, Dobrovolskaya TG (2002) Fungal and bacterial communities in Lumbricus terrestris burrow walls. A laboratory experiment. Pedobiologia 46:595–605
Tiunov AV, Scheu S (1999) Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris. Soil Biol Biochem 31:2039–2048
Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537
Uksa M, Fischer D, Welzl G, Kautz T, Köpke U, Schloter M (2014) Community structure of prokaryotes and their functional potential in subsoils is more affected by spatial heterogeneity than by temporal variations. Soil Biol Biochem 75:197–201
van Groenigen JW, Lubbers IM, Vos HMJ, Brown GG, de Deyn GB, van Groenigen KJ (2014) Earthworms increase plant production: a meta-analysis. Scientific reports 4:6365
Vetterlein D, Kühn T, Kaiser K, Jahn R (2013) Illite transformation and potassium release upon changes in composition of the rhizophere soil solution. Plant Soil 371:267–279
Volkmar KM (1996) Effects of biopores on the growth and N-uptake of wheat at three levels of soil moisture. Can J Soil Sci 76:453–458
von Luetzow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (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
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554
Waldrop M, Balser T, Firestone M (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846
Werth M, Kuzyakov Y (2010) 13C fractionation at the root–microorganisms–soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384
White GF, Russell NJ, Tidswell EC (1996) Bacterial scission of ether bonds. Microbiol Rev 60:216–232
Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Experimental and theoretical approaches in environmental chemistry. Chemosphere 35:275–294
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129
Zhang X, Amelung W (1996) Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem 28:1201–1206
Zhang H, Schrader S (1993) Earthworm effects on selected physical and chemical properties of soil aggregates. Biol Fertil Soils 15:229–234
Zhou J, Xia B, Treves DS, Wu L-Y, Marsh TL, O'Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334
Acknowledgements
This study was supported by the German Research Foundation, grants DFG KU 1184/29-1 and INST 186/1006-1. We would like to thank PD Dr. Timo Kautz and the colleagues from the Institute of Organic Agriculture of the University of Bonn for establishing and managing the field trial Klein-Altendorf, as well as the Centre for Stable Isotope Research and Analysis, Goettingen, for δ13C determination.
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Table S1
Full PLFA dataset: given are PLFA amounts in μg per g dry soil for each pore type and bulk soil for two soil depths (DOCX 28 kb).
Table S2
Full amino sugar dataset: given are PLFA amounts in μg per g dry soil for each pore type and bulk soil for two soil depths (DOCX 22 kb).
Table S3
PLFA amounts of fresh earthworm casts, given in μg per g dry material (DOCX 21 kb).
Fig S4
Principal component analysis of the PLFA dataset, without rotation. (GIF 218 kb).
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Banfield, C.C., Dippold, M.A., Pausch, J. et al. Biopore history determines the microbial community composition in subsoil hotspots. Biol Fertil Soils 53, 573–588 (2017). https://doi.org/10.1007/s00374-017-1201-5
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DOI: https://doi.org/10.1007/s00374-017-1201-5