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Reinoculation elucidates mechanisms of bacterial community assembly in soil and reveals undetected microbes

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Abstract

Soils harbor a huge diversity of microorganisms that participate in various biogeochemical cycles and influence soil fertility. Our knowledge of soil microbiota, however, is limited by the complexity and heterogeneity of soil habitats and the huge microbial diversity. In this study, fertilized and unfertilized soils from a long-term fertilization experiment were gamma-sterilized before self- or cross-inoculation with non-sterilized soil aliquots containing their respective microbial communities. Bacterial community dynamics resulting from each reinoculated treatment was monitored over 90 days using B-ARISA. This study design allowed us to assess the respective influences of two driving factors, original community and soil nutrient availability, on microbial community assemblage dynamics. For all treatments, the bacterial communities that evolved in the sterilized soils differed from those in the original soils and displayed dynamic shifts over time. These shifts were particularly illustrated by the appearance of numerous OTUs that were undetectable in the original soils and suggest that community assembly is primarily determined by niche factors. However, stronger community shifts and higher variations among the replicates were observed after reinoculation of nutrient-rich soil, suggesting an increased impact of stochastic processes on community assembly. Our results demonstrate that reinoculation-based approaches are not only valid for detecting a variety of low abundant soil bacteria but also for distinguishing the soil characteristics and ecological rules that shape soil microbial population assemblage.

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References

  • Bell CH (2000a) Fumigation in the 21st century. Crop Protect 19:563–569

    Article  CAS  Google Scholar 

  • Bell G (2000b) The distribution of abundance in neutral communities. Am Nat 155:606–617. doi:10.1086/303345

    Article  PubMed  Google Scholar 

  • Bell G (2001) Neutral Macroecology Science 293:2413–2418

    CAS  PubMed  Google Scholar 

  • Birkhofer K, Schoening I, Alt F, Herold N, Klarner B, Maraun M, Marhan S, Oelmann Y, Wubet T, Yurkov A, Begerow D, Berner D, Buscot F, Daniel R, Diekoetter T, Ehnes RB, Erdmann G, Fischer C, Foesel B, Groh J, Gutknecht J, Kandeler E, Lang C, Lohaus G, Meyer A, Nacke H, Naether A, Overmann J, Polle A, Pollierer MM, Scheu S, Schloter M, Schulze E-D, Schulze W, Weinert J, Weisser WW, Wolters V, Schrumpf M (2012) General relationships between abiotic soil properties and soil biota across spatial scales and different land-use types. Plos One 7(8):e43292. doi:10.1371/journal.pone.0043292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borneman J, Triplett EW (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63:2647–2653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowen HJM, Cawse PA (1964) Some effects of Gamma radiation on the composition of the soil solution and soil organic matter. Soil Sci 98:358–361

    Article  CAS  Google Scholar 

  • Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240

    Article  CAS  Google Scholar 

  • Cortois R, De Deyn G (2012) The curse of the black box. Plant Soil 350:27–33. doi:10.1007/s11104-011-0963-z

    Article  CAS  Google Scholar 

  • Coveley S, Elshahed MS, Youssef NH (2015) Response of the rare biosphere to environmental stressors in a highly diverse ecosystem (Zodletone Spring, OK, USA). PeerJ 3:e1182. doi:10.7717/peerj.1182

    Article  PubMed  PubMed Central  Google Scholar 

  • Crump BC, Amaral-Zettler LA, Kling GW (2012) Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J 6:1629–1639. doi:10.1038/ismej.2012.9

    Article  CAS  PubMed  PubMed Central  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 Fertil Soils 50:1069–1076. doi:10.1007/s00374-014-0925-8

    Article  CAS  Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345

    Article  PubMed  Google Scholar 

  • Elshahed MS, Youssef NH, Spain AM, Sheik C, Najar FZ, Sukharnikov LO, Roe BA, Davis JP, Schloss PD, Bailey VL, Krumholz LR (2008) Novelty and uniqueness patterns of rare members of the soil biosphere. Appl Environ Microbiol 74:5422–5428. doi:10.1128/AEM.00410-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631. doi:10.1073/pnas.0507535103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. doi:10.1890/05-1839

    Article  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Francioli D, Ascher J, Ceccherini MT, Pietramellara G (2014) Land use and seasonal effects on a Mediterranean soil bacterial community. J Soil Sci Plant Nutr 14:710–722

    Google Scholar 

  • Frossard A, Gerull L, Mutz M, Gessner MO (2012) Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors. Isme J 6:680–691

    Article  CAS  PubMed  Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390. doi:10.1126/science.1112665

    Article  CAS  PubMed  Google Scholar 

  • Gleeson D, Clipson N, Melville K, Gadd G, McDermott F (2005) Characterization of fungal community structure on a weathered pegmatitic granite. Microb Ecol 50:360–368. doi:10.1007/s00248-005-0198-8

    Article  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9

    Google Scholar 

  • Hartmann M, Frey B, Mayer J, Mader P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. Isme J 9:1177–1194. doi:10.1038/ismej.2014.210

    Article  PubMed  Google Scholar 

  • Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. doi:10.1038/nrmicro2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbell SP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87:1387–1398

    Article  PubMed  Google Scholar 

  • Insam H (2001) Developments in soil microbiology since the mid 1960s. Geoderma 100:389–402. doi:10.1016/S0016-7061(01)00029-5

    Article  CAS  Google Scholar 

  • Jones SE, Shade AL, Mcmahon KD, Kent AD (2007) Comparison of primer sets for use in automated ribosomal intergenic spacer analysis of aquatic bacterial communities: an ecological perspective. Appl Environ Microbiol 73:659–662. doi:10.1128/aem.02130-06

    Article  CAS  PubMed  Google Scholar 

  • Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130

    Article  CAS  PubMed  Google Scholar 

  • Lensi R, Lescure C, Steinberg C, Savoie JM, Faurie G (1991) Dynamics of residual enzyme activities, denitrification potential, and physico-chemical properties in a γ-sterilized soil. Soil Biol Biochem 23:367–373. doi:10.1016/0038-0717(91)90193-N

    Article  CAS  Google Scholar 

  • Lotrario JB, Stuart BJ, Lam T, Arands RR, O’Connor OA, Kosson DS (1995) Effects of sterilization methods on the physical characteristics of soil: implications for sorption isotherm analyses. Bull Environ Contam Toxicol 54:668–675. doi:10.1007/BF00206097

    Article  CAS  PubMed  Google Scholar 

  • Macarthur R (1970) Species packing and competitive equilibrium for many species. Theor Popul Biol 1:1–11. doi:10.1016/0040-5809(70)90039-0

    Article  CAS  PubMed  Google Scholar 

  • Mallon CA, Poly F, Le Roux X, Marring I, van Elsas JD, Salles JF (2015) Resource pulses can alleviate the biodiversity–invasion relationship in soil microbial communities. Ecology 96:915–926. doi:10.1890/14-1001.1

    Article  PubMed  Google Scholar 

  • Mcnamara NP, Black HIJ, Beresford NA, Parekh NR (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24:117–132. doi:10.1016/S0929-1393(03)00073-8

    Article  Google Scholar 

  • Merbach I, Schulz E (2012) Long-term fertilization effects on crop yields, soil fertility and sustainability in the static fertilization experiment bad lauchstädt under climatic conditions 2001–2011. Archives of Agronomy and Soil Science 59:1041–1057. doi:10.1080/03650340.2012.702895

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. doi:10.1016/S0003-2670(00)88444-5

    Article  CAS  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. doi:10.1046/j.1351-0754.2003.0556.x

    Article  Google Scholar 

  • Nicolardot B, Bouziri L, Bastian F, Ranjard L (2007) A microcosm experiment to evaluate the influence of location and quality of plant residues on residue decomposition and genetic structure of soil microbial communities. Soil Biol Biochem 39:1631–1644. doi:10.1016/j.soilbio.2007.01.012

    Article  CAS  Google Scholar 

  • Pester M, Bittner N, Deevong P, Wagner M, Loy A (2010) A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland. Isme J 4:1591–1602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pietramellara G, Ascher J, Ceccherini MT, Renella G (2002) Soil as a biological system. Ann Microbiol 52:119–131

    Google Scholar 

  • Pontarp M, Canbäck B, Tunlid A, Lundberg P (2012) Phylogenetic analysis suggests that habitat filtering is structuring marine bacterial communities across the globe. Microb Ecol 64:8–17. doi:10.1007/s00248-011-0005-7

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Progress 13:959–964. doi:10.1007/s11557-013-0954-y

    Article  Google Scholar 

  • Purahong W, Stempfhuber B, Lentendu G, Francioli D, Reitz T, Buscot F, Schloter M, Kruger D (2015) Influence of commonly used primer systems on automated ribosomal intergenic spacer analysis of bacterial communities in environmental samples. PLoS One 10:e0118967. doi:10.1371/journal.pone.0118967

    Article  PubMed  PubMed Central  Google Scholar 

  • R core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/. Accessed 24 Sept 2012.

  • 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  PubMed Central  Google Scholar 

  • Ramsay AJ, Bawden AD (1983) Effects of sterilization and storage on respiration, nitrogen status and direct counts of soil bacteria using acridine orange. Soil Biol Biochem 15:263–268. doi:10.1016/0038-0717(83)90069-X

    Article  CAS  Google Scholar 

  • Ranjard L, Poly F, Lata J-C, 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  PubMed Central  Google Scholar 

  • Riehm H (1945) Die bestimmung des phosphorsaure und kalibedarfs der ackerboden. Angew Chem-Ger Edit 58:73–76

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schulz E (2002) Influence of extreme management on decomposable soil organic matter pool. Archives of Agronomy and Soil Science 48:101–105. doi:10.1080/03650340214166

    Article  Google Scholar 

  • Shade A, Peter H, Allison SD, Baho DL, Berga M, Burgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417. doi:10.3389/fmicb.2012.00417

    Article  PubMed  PubMed Central  Google Scholar 

  • Shade A, Jones SE, Caporaso JG, Handelsman J, Knight R, Fierer N, Gilbert JA (2014) Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio 5:e01371–01314. doi:10.1128/mBio.01371-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Sørensen J, Haubjerg Nicolaisen M, Ron E, Simonet P (2009) Molecular tools in rhizosphere microbiology—from single-cell to whole-community analysis. Plant Soil 321:483–512. doi:10.1007/s11104-009-9946-8

    Article  Google Scholar 

  • Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Article  Google Scholar 

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Nat Acad Sci USA 101:10854–10861. doi:10.1073/pnas.0403458101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066. doi:10.1126/science.1071698

    Article  CAS  PubMed  Google Scholar 

  • Turelli M (1981) Niche overlap and invasion of competitors in random environments. I. Models without demographic stochasticity. Theor Popul Biol 20:1–56. doi:10.1016/0040-5809(81)90002-2

    Article  Google Scholar 

  • Vuono DC, Munakata-Marr J, Spear JR, Drewes JE (2016) Disturbance opens recruitment sites for bacterial colonization in activated sludge. Environ Microbiol 18:87–99. doi:10.1111/1462-2920.12824

    Article  CAS  PubMed  Google Scholar 

  • Weig AR, Peršoh D, Werner S, Betzlbacher A, Rambold G (2013) Diagnostic assessment of mycodiversity in environmental samples by fungal ITS1 rDNA length polymorphism. Mycol Progress 12:719–725. doi:10.1007/s11557-012-0883-1

    Article  Google Scholar 

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Acknowledgments

This study was financially supported by the HIGRADE PhD scholarship of Davide Francioli and by special funds provided by the Helmholtz Centre for Environmental Research - UFZ. We wish to thank Ines Merbach and the workers of the Bad Lauchstädt research station for their support during soil sampling and Gabriele Henning, Jacqueline Rose, and Renate Rudloff for kindly providing the soil parameters. We are also grateful to Caterina Maggi for her assistance.

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  1. Department of Soil Ecology, UFZ-Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle (Saale), Germany

    Davide Francioli, Elke Schulz, Witoon Purahong, François Buscot & Thomas Reitz

  2. German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany

    François Buscot & Thomas Reitz

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  1. Davide Francioli
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  2. Elke Schulz
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Correspondence to Davide Francioli.

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Table S1 Mean values of the number of OTUs detected in each treatment. Fig. S1 Schematic representation of the microcosm experimental setup adopted in this work. Fig. S2 Bacterial richness observed in all soil treatments investigated during the experiment. No significant changes in richness were observed among all the treatments and/or over time according to Fischer’s LSD test p < 0.05. Fig. S3 Venn diagrams showing specific and common bacterial OTUs between the reinoculated microcosms (uU, uF, fU, and fF), and the original soils (U-0 and F-0) after (a) 25 days and (b) 90 days from the beginning of the experiment. Fig. S4 Venn diagrams showing specific and common bacterial OTUs among the same treatments at different time points (after 25 days and 90 days). (PDF 413 kb)

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Francioli, D., Schulz, E., Purahong, W. et al. Reinoculation elucidates mechanisms of bacterial community assembly in soil and reveals undetected microbes. Biol Fertil Soils 52, 1073–1083 (2016). https://doi.org/10.1007/s00374-016-1141-5

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