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Resource Type and Availability Regulate Fungal Communities Along Arable Soil Profiles

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Abstract

Soil fungi play an essential role in the decomposition of plant-derived organic material entering soils. The quality and quantity of organic compounds vary seasonally as well as with soil depth. To elucidate how these resources affect fungal communities in an arable soil, a field experiment was set up with two plant species, maize and wheat. Resource availability was experimentally manipulated by maize litter input on one half of these maize and wheat plots after harvest in autumn. Fungal biomass was determined by ergosterol quantification, and community structure was investigated by fungal automated ribosomal intergenic spacer analysis (F-ARISA). An annual cycle was assessed across a depth gradient, distinguishing three soil habitats: the plough layer, rooted soil below the plough layer, and deeper root-free soil. Fungal communities appeared highly dynamic and varied according to soil depth and plant resources. In the plough layer, the availability of litter played a dominant role in shaping fungal communities, whereas in the rooted layer below, community structure and biomass mainly differed between plant species. This plant effect was also extended into the root-free soil at a depth of 70 cm. In winter, the availability of litter also affected fungal communities in deeper soil layers, suggesting vertical transport processes under fallow conditions. These distinct resource effects indicate diverse ecological niches along the soil profile, comprising specific fungal metacommunities. The recorded responses to both living plants and litter point to a central role of fungi in connecting primary production and decomposition within the plant-soil system.

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References

  1. Bridge P, Spooner B (2001) Soil fungi: diversity and detection. Plant Soil 232:147–154. doi:10.1023/A:1010346305799

    Article  CAS  Google Scholar 

  2. Buscot F, Varma A (2005) Microorganisms in soils: roles in genesis and functions. Springer, Germany

    Google Scholar 

  3. Christensen M (1989) A View of Fungal Ecology. Mycologia 81:1–19. doi:10.2307/3759446

    Article  Google Scholar 

  4. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811. doi:10.1016/j.femsre.2004.11.005

    Article  PubMed  Google Scholar 

  5. Frey SD, Six J, Elliott ET (2003) Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil-litter interface. Soil Biol Biochem 35:1001–1004. doi:10.1016/S0038-0717(03)00155-X

    Article  CAS  Google Scholar 

  6. Kramer C, Gleixner G (2006) Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biol Biochem 38:3267–3278. doi:10.1016/j.soilbio.2006.04.006

    Article  CAS  Google Scholar 

  7. 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. doi:10.1016/S0038-0717(01)00158-4

    Article  Google Scholar 

  8. Luo ZK, Wang EL, Sun OJ (2010) Can no-tillage stimulate carbon sequestration in agricultural soils? A meta-analysis of paired experiments. Agric Ecosyst Environ 139:224–231. doi:10.1016/j.agee.2010.08.006

    Article  CAS  Google Scholar 

  9. Yan Y, Tian J, Fan MS, Zhang FS, Li XL, Christie P, Chen HQ, Lee J, Kuzyakov Y, Six J (2012) Soil organic carbon and total nitrogen in intensively managed arable soils. Agric Ecosyst Environ 150:102–110. doi:10.1016/j.agee.2012.01.024

    Article  CAS  Google Scholar 

  10. Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: A review. Soil Sci 165:277–304. doi:10.1097/00010694-200004000-00001

    Article  CAS  Google Scholar 

  11. Majdalani S, Michel E, Di-Pietro L, Angulo-Jaramillo R (2008) Effects of wetting and drying cycles on in situ soil particle mobilization. Eur J Soil Sci 59:147–155. doi:10.1111/j.1365-2389.2007.00964.x

    Article  Google Scholar 

  12. 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. doi:10.1007/s11104-010-0391-5

    Article  CAS  Google Scholar 

  13. Totsche KU, Jann S, Kögel-Knabner I (2007) Single event-driven export of polycyclic aromatic hydrocarbons and suspended matter from coal tar-contaminated soil. Vadose Zone J 6:233–243. doi:10.2136/Vzj2006.0083

    Article  CAS  Google Scholar 

  14. Debosz K, Rasmussen PH, Pedersen AR (1999) Temporal variations in microbial biomass C and cellulolytic enzyme activity in arable soils: effects of organic matter input. Appl Soil Ecol 13:209–218. doi:10.1016/S0929-1393(99)00034-7

    Article  Google Scholar 

  15. Kaye JP, McCulley RL, Burke IC (2005) Carbon fluxes, nitrogen cycling, and soil microbial communities in adjacent urban, native and agricultural ecosystems. Glob Chang Biol 11:575–587. doi:10.1111/j1365-2486.2005.00921.x

    Article  Google Scholar 

  16. Rochette P, Angers DA, Flanagan LB (1999) Maize residue decomposition measurement using soil surface carbon dioxide fluxes and natural abundance of carbon-13. Soil Sci Soc Am J 63:1385–1396. doi:10.2136/sssaj1999.6351385x

    Article  CAS  Google Scholar 

  17. Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148. doi:10.1055/s-2001-12905

    Article  CAS  Google Scholar 

  18. Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1167. doi:10.1007/s10021-008-9186-4

    Article  CAS  Google Scholar 

  19. Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135. doi:10.1111/j.1461-0248.2006.00965.x

    Article  PubMed  Google Scholar 

  20. Kramer S, Marhan S, Haslwimmer H, Ruess L, Kandeler E (2013) Temporal variation in surface and subsoil abundance and function of the soil microbial community in an arable soil. Soil Biol Biochem 61:76–85. doi:10.1016/j.soilbio.2013.02.006

    Article  CAS  Google Scholar 

  21. Hannula SE, de Boer W, van Veen J (2012) A 3-year study reveals that plant growth stage, season and field site affect soil fungal communities while cultivar and GM-trait have minor effects. PLoS One 7:e33819. doi:10.1371/journal.pone.0033819

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Jumpponen A, Jones KL, Blair J (2010) Vertical distribution of fungal communities in tallgrass prairie soil. Mycologia 102:1027–1041. doi:10.3852/09-316

    Article  PubMed  Google Scholar 

  23. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. doi:10.1128/AEM. 02188-07

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Chigineva NI, Aleksandrova AV, Tiunov AV (2009) The addition of labile carbon alters litter fungal communities and decreases litter decomposition rates. Appl Soil Ecol 42:264–270. doi:10.1016/j.apsoil.2009.05.001

    Article  Google Scholar 

  25. Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285. doi:10.1016/j.ecolecon.2007.03.004

    Article  Google Scholar 

  26. Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283. doi:10.1111/j.1469-8137.2004.01235.x

    Article  PubMed  Google Scholar 

  27. Verbruggen E, Van Der Heijden MG, Weedon JT, Kowalchuk GA, Roling WF (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21:2341–2353. doi:10.1111/j.1365-294X.2012.05534.x

    Article  PubMed  Google Scholar 

  28. de Castro AP, Quirino BF, Pappas G Jr, Kurokawa AS, Neto EL, Kruger RH (2008) Diversity of soil fungal communities of Cerrado and its closely surrounding agriculture fields. Arch Microbiol 190:129–139. doi:10.1007/s00203-008-0374-6

    Article  CAS  PubMed  Google Scholar 

  29. Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendona-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766. doi:10.1128/aem. 69.7.3758-3766.2003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Klaubauf S, Inselsbacher E, Zechmeister-Boltenstern S, Wanek W, Gottsberger R, Strauss J, Gorfer M (2010) Molecular diversity of fungal communities in agricultural soils from Lower Austria. Fungal Divers 44:65–75. doi:10.1007/s13225-010-0053-1

    Article  PubMed Central  PubMed  Google Scholar 

  31. Xu L, Ravnskov S, Larsen J, Nicolaisen M (2012) Linking fungal communities in roots, rhizosphere, and soil to the health status of Pisum sativum. FEMS Microbiol Ecol 82:736–745. doi:10.1111/j.1574-6941.2012.01445.x

    Article  CAS  PubMed  Google Scholar 

  32. Kramer S, Marhan S, Ruess L, Armbruster W, Butenschoen O, Haslwimmer H, Kuzyakov Y, Pausch J, Scheunemann N, Schoene J, Schmalwasser A, Totsche KU, Walker F, Scheu S, Kandeler E (2012) Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 55:111–119. doi:10.1016/j.pedobi.2011.12.001

    Article  CAS  Google Scholar 

  33. Pausch J, Kuzyakov Y (2012) Soil organic carbon decomposition from recently added and older sources estimated by delta C-13 values of CO2 and organic matter. Soil Biol Biochem 55:40–47. doi:10.1016/j.soilbio.2012.06.007

    Article  CAS  Google Scholar 

  34. Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Ranjard L, Poly F, Lata JC, Mougel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: Biological and methodological variability. Appl Environ Microbiol 67:4479–4487. doi:10.1128/Aem. 67.10.4479-4487.2001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Corneo PE, Pellegrini A, Cappellin L, Gessler C, Pertot I (2014) Moderate warming in microcosm experiment does not affect microbial communities in temperate vineyard soils. Microb ecol: 1-12. doi: 10.1007/s00248-013-0357-2

  37. Frossard A, Gerull L, Mutz M, Gessner MO (2013) Shifts in microbial community structure and function in stream sediments during experimentally simulated riparian succession. FEMS Microbiol Ecol 84:398–410. doi:10.1111/1574-6941.12072

    Article  CAS  PubMed  Google Scholar 

  38. Purahong W, Kahl T, Schloter M, Bauhus J, Buscot F, Krüger D (2014) Comparing fungal richness and community composition in coarse woody debris in Central European beech forests under three types of management. Mycol Prog: 1-6. doi: 10.1007/s11557-013-0954-y

  39. Scharroba A, Dibbern D, Hünninghaus M, Kramer S, Moll J, Butenschoen O, Bonkowski M, Buscot F, Kandeler E, Koller R, Krüger D, Lueders T, Scheu S, Ruess L (2012) Effects of resource availability and quality on the structure of the micro-food web of an arable soil across depth. Soil Biol Biochem 50:1–11. doi:10.1016/j.soilbio.2012.03.002

    Article  CAS  Google Scholar 

  40. Djajakirana G, Joergensen RG, Meyer B (1996) Ergosterol and microbial biomass relationship in soil. Biol Fertil Soils 22:299–304. doi:10.1007/Bf00334573

    Article  CAS  Google Scholar 

  41. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75:2495–2505. doi:10.1128/AEM. 02409-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. ISBN 3-900051-07-0, Vienna, Austria

  43. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x

    Google Scholar 

  44. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O'Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2011) vegan: Community Ecology Package. R package version 2.0-2

  45. Yannarell AC, Busby RR, Denight ML, Gebhart DL, Taylor SJ (2011) Soil bacteria and fungi respond on different spatial scales to invasion by the legume Lespedeza cuneata. Front Microbiol 2:127. doi:10.3389/fmicb.2011.00127

    Article  PubMed Central  PubMed  Google Scholar 

  46. Yannarell AC, Menning SE, Beck AM (2014) Influence of shrub encroachment on the soil microbial community composition of remnant hill prairies. Microb ecol: 1-10. doi: 10.1007/s00248-014-0369-6

  47. Hartmann M, Lee S, Hallam SJ, Mohn WW (2009) Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environ Microbiol 11:3045–3062. doi:10.1111/j.1462-2920.2009.02008.x

    Article  PubMed  Google Scholar 

  48. O'Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550. doi:10.1128/Aem. 71.9.5544-5550.2005

    Article  PubMed Central  PubMed  Google Scholar 

  49. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176. doi:10.1016/S0038-0717(02)00251-1

  50. Beauregard MS, Hamel C, Atul N, St-Arnaud M (2010) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol 59:379–389. doi:10.1007/s00248-009-9583-z

    Article  CAS  PubMed  Google Scholar 

  51. Helgason BL, Walley FL, Germida JJ (2010) No-till soil management increases microbial biomass and alters community profiles in soil aggregates. Appl Soil Ecol 46:390–397. doi:10.1016/j.apsoil.2010.10.002

    Article  Google Scholar 

  52. Burges A, Fenton E (1953) The effect of carbon dioxide on the growth of certain soil fungi. Trans Br Mycol Soc 36:104–108. doi:10.1016/S0007-1536(53)80054-9

    Article  CAS  Google Scholar 

  53. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58

    Article  PubMed  Google Scholar 

  54. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. doi:10.1016/j.soilbio.2008.05.021

    Article  CAS  Google Scholar 

  55. McGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: Decomposition as a case study. Soil Biol Biochem 42:529–535. doi:10.1016/j.soilbio.2009.11.016

    Article  CAS  Google Scholar 

  56. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762. doi:10.1038/ismej.2012.11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Baldrian P, Voriskova J, Dobiasova P, Merhautova V, Lisa L, Valaskova V (2011) Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338:111–125. doi:10.1007/s11104-010-0324-3

    Article  CAS  Google Scholar 

  58. van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev 37:477–494. doi:10.1111/1574-6976.12001

    Article  PubMed  Google Scholar 

  59. Trinder CJ, Johnson D, Artz RR (2009) Litter type, but not plant cover, regulates initial litter decomposition and fungal community structure in a recolonising cutover peatland. Soil Biol Biochem 41:651–655. doi:10.1016/j.soilbio.2008.12.006

    Article  CAS  Google Scholar 

  60. Pausch J, Tian J, Riederer M, Kuzyakov Y (2012) Estimation of rhizodeposition at field scale: upscaling of a 14 C labeling study. Plant Soil 1–13. doi:10.1007/s11104-012-1363-8

  61. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. doi:10.1111/j.1574-6941.2009.00654.x

    Article  CAS  PubMed  Google Scholar 

  62. Fan TWM, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57:209–221. doi:10.1016/S0031-9422(01)00007-3

    Article  CAS  PubMed  Google Scholar 

  63. Singh BK, Dawson LA, Macdonald CA, Buckland SM (2009) Impact of biotic and abiotic interaction on soil microbial communities and functions: a field study. Appl Soil Ecol 41:239–248. doi:10.1016/j.apsoil.2008.10.003

    Article  Google Scholar 

  64. Miller RM, Fitzsimons MS (2011) Fungal growth in soils. In: Ritz K, Young I (eds) The architecture and biology of soils: Life in inner space. Cabi International, London, pp 149–163

    Chapter  Google Scholar 

  65. Dibbern D, Schmalwasser A, Lueders T, Totsche KU (2014) Selective transport of plant root-associated bacterial populations in agricultural soils upon snowmelt. Soil Biol Biochem 69:187–196. doi:10.1016/j.soilbio.2013.10.040

    Article  CAS  Google Scholar 

  66. Natsch A, Keel C, Troxler J, Zala M, VonAlbertini N, Defago G (1996) Importance of preferential flow and soil management in vertical transport of a biocontrol strain of Pseudomonas fluorescens in structured field soil. Appl Environ Microbiol 62:33–40

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Bissinger V, Kolditz O (2008) Helmholtz Interdisciplinary Graduate School for Environmental Research (HIGRADE). Gaia 17:71–73

    Google Scholar 

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Acknowledgments

We thank Olaf Butenschoen for management at the field site and the many field work helpers. Björn Hoppe is gratefully acknowledged for providing his expertise on F-ARISA analysis and Renate Rudloff for her technical assistance during laboratory work. This study was performed within the framework of the Research Unit “Carbon flow in belowground food webs assessed by isotope tracers” of the DFG (FOR 918) and was also supported by Helmholtz Impulse and Networking Fund through Helmholtz Interdisciplinary Graduate School for Environmental Research (HIGRADE) [67].

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Moll, J., Goldmann, K., Kramer, S. et al. Resource Type and Availability Regulate Fungal Communities Along Arable Soil Profiles. Microb Ecol 70, 390–399 (2015). https://doi.org/10.1007/s00248-015-0569-8

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