Microbial Ecology

, Volume 72, Issue 3, pp 717–724 | Cite as

Bacterial Community Structure at the Microscale in Two Different Soils

  • Rory Michelland
  • Jean Thioulouse
  • Martina Kyselková
  • Genevieve L. GrundmannEmail author
Soil Microbiology


The spatial distributions of bacteria in the soil matrix have a role in ecosystem function, for example, at the small scale, through gene transfer or xenobiotic degradation. Soil bacterial biogeography has been evidenced at the large scale, but data are scarce at the small scale. The objective of this work was to determine the spatial pattern of bacterial diversity, in spatially referenced microsamples, in order to define bacterial community spatial traits. Two soils with different physical structures, moderately aggregated (La Côte St André (LCSA)) or poorly aggregated (La Dombes (LD)), were studied. The spatial distribution of bacteria was studied in microsamples (diameter 3 mm) along 10- and 20-cm transects, with a taxonomic microarray. 16S rRNA gene sequencing was used to further study the spatial characteristics of the microbial communities in LD soil. The frequency-occupancy plot, in the LCSA and LD soils, using microarray and sequencing data, followed Hanski’s core-satellite theory. The frequency-occupancy distribution plots obtained in two different soils showed bimodality and indicated that the microscale spatial distributions were different, particularly core taxa percentage. Core taxa are widespread and abundant, while satellite taxa are restricted in their distribution. The spread of satellite taxa was at a distance range larger than 5 cm, whereas the core taxa were distributed in a distance range less than 3 mm. Besides, there was a positive abundancy-occupancy relationship at this fine scale. It may be interesting to further evaluate the role of the different bacterial spatial distributions at the fine scale on soil function.


Abundancy-occupancy relationship Bacteria community structure Microscale in soil Frequency-occupancy relationship Soil microbial diversity Soil structure 



For their involvement with sample processing, we thank Florent Gaudel and Jacqueline Haurat. Audrey Dubost helped with data processing. We thank Naoise Nunan for his valuable comments and suggestions on the manuscript.

This work was supported by the Specific Internal Program of the UMR 5557 Ecologie Microbienne.

Compliance with ethical standards

We confirm that all of the reported work is original. The material has not been submitted for publication elsewhere.

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

248_2016_810_MOESM1_ESM.xlsx (11 kb)
Table S1 LCSA and LD soils physico-chemical characteristics. (XLSX 11 kb)
248_2016_810_MOESM2_ESM.doc (320 kb)
Table S2 Core and satellite taxa found in LD soil with 16S rDNA gene pyrosequencing and in LCSA and LD soil with microarray analysis. (DOC 319 kb)


  1. 1.
    Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL et al (2006) Microbial biogeography: putting microorganisms on the map. Nature Rev Microbiol 4:102–112CrossRefGoogle Scholar
  2. 2.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Cho JC, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66:5448–5456CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Noguez AM, Arita HT, Escalante AE, Forney LJ, Garcia-Oliva F, Souza V (2005) Microbial macro-ecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest. Global Ecol Biogeogr 14:241–248CrossRefGoogle Scholar
  5. 5.
    Franklin RB, Blum LK, Mc Comb A, Mills AL (2002) A geostatistical analysis of small-scale spatial variability in bacterial abundance and community structure in salt marsh creek bank sediments. FEMS Microbiol Ecol 42:71–80CrossRefPubMedGoogle Scholar
  6. 6.
    Oda Y, Star B, Huisman LA, Gottschal JC, Forney LJ (2003) Biogeography of the purple nonsulfur bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 69:5186–5191CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ovreas L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373PubMedPubMedCentralGoogle Scholar
  8. 8.
    Ettema C, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evolut 17:177–183CrossRefGoogle Scholar
  9. 9.
    Vilas Boas G, Sanchis V, Lereclus D, Lemos MV, Bourquet D (2002) Genetic differentiation between sympatric populations of Bacillus cereus and Bacillus thuringiensis. Appl Environ Microbiol 68:1414–1424CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Grundmann GL, Debouzie D (2000) Geostatistical analysis of the distribution of NH4 + and NO2 -oxidizing bacteria and serotypes at the millimeter scale along a soil transect. FEMS Microbiol Ecol 34:57–62PubMedGoogle Scholar
  11. 11.
    Becker JM, Parkin T, Nakatsu CH, Wilbur JD, Konopka A (2006) Bacterial activity, community structure and centimeter-scale spatial heterogeneity in contaminated soils. Microbiol Ecol 51:220–231CrossRefGoogle Scholar
  12. 12.
    Stefanic P, Mandic-Mulec I (2009) Social interactions and distribution of Bacillus subtilis pherotypes at microscale. J Bacteriol 191:1756–1764CrossRefPubMedGoogle Scholar
  13. 13.
    Bailey VL, Bilskis CL, Fansler SJ, McCue LA, Smith JL, Konopka A (2012) Measurements of microbial community activities in individual soil macroaggregates. Soil Biol Biochem 48:192–195CrossRefGoogle Scholar
  14. 14.
    Kim H, Nunan N, Dechesne A, Juarez S, Grundmann GL (2015) The spatial distribution of exoenzyme activities across the soil micro-landscape, as measured in micro-and macro-aggregates, and ecosystem processes. Soil Biol Biochem 91:258–267Google Scholar
  15. 15.
    Young IM, Crawford JW, Nunan N, Otten W, Spiers A (2008) Microbial distribution in soils: physics and scaling. Adv Agron 100:81–121CrossRefGoogle Scholar
  16. 16.
    Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  17. 17.
    Pallud C, Dechesne A, Gaudet JP, Debouzie D, Grundmann GL (2004) Modification of spatial distribution of 2,4-dichloro-phenoxyacetic acid degrader microhabitats during growth in soil columns. Appl Environ Microbiol 70:2709–2716CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Vieublé Gonod L, Chadoeuf J, Chenu C (2006) Spatial distribution of microbial 2,4 dichlorophenoxy acetic acid mineralization from field to microhabitat scales. Soil Sci Soc Am J 70:64–71CrossRefGoogle Scholar
  19. 19.
    Youssef NH, Couger MB, Elshahed MS (2010) Fine-scale bacterial diversity within a complex ecosystem (Zodletone Spring, OK, USA): the role of the rare biosphere. PloS One 5(8):e12414CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ranjard L, Richaume A, Jocteur-Monrozier L, Nazaret S (1997) Response of soil bacteria to Hg(II) in relation to soil characteristics and cell location. FEMS Microbiol Ecol 24:321–331CrossRefGoogle Scholar
  21. 21.
    Orsiny M, Romano-Spica V (2001) A microwave-based method for nucleic acid isolation from environmental samples. Lettr Appl Microbiol 33:17–20CrossRefGoogle Scholar
  22. 22.
    Sanguin H, Remenant B, Dechesne A, Thioulouse J, Vogel TM, Nesme X et al (2006) Potential of a 16S rRNA-based taxonomic microarray for analyzing the rhizosphere effects of maize on Agrobacterium spp. and bacterial communities. Appl Environ Microbiol 72:4302–4312CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Kyselková M, Kopecký J, Frapoli M, Défago G, Ságová-Marečková M et al (2009) Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black rot disease. ISMEJ 3:1127–1138CrossRefGoogle Scholar
  24. 24.
    Sanguin H, Herrera A, Oger C, Dechesne A, Simonet P, Navarro E et al (2006) Development and validation of a prototype 16S rRNA-based taxonomic microarray for Alphaproteobacteria. Environ Microbiol 8:289–307CrossRefPubMedGoogle Scholar
  25. 25.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–72CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graphical Stat 5:299–314Google Scholar
  27. 27.
    R Core Team (2016). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  28. 28.
    Thioulouse J, Dray S (2007) Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. J Stat Softw 22(5):1–14CrossRefGoogle Scholar
  29. 29.
    Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221CrossRefGoogle Scholar
  30. 30.
    Hanski I, Gyllenberg M (1997) Uniting two general patterns in the distribution of species. Science 275:397–400CrossRefPubMedGoogle Scholar
  31. 31.
    Ulrich W, Zalewski M (2006) Abundance and co-occurrence patterns of core and satellite species of ground beetles on small lake islands. Oikos 114:338–348CrossRefGoogle Scholar
  32. 32.
    Heatherly T, Whiles MR, Gibson DJ, Collins SL, Huryn AD, Jackson JK, Palmer MA (2007) Stream insect occupancy-frequency patterns and metapopulation structure. Oecologia 151:313–321CrossRefPubMedGoogle Scholar
  33. 33.
    Magurran AE (2007) Species abundance distributions over time. Ecol Lett 10:347–354CrossRefPubMedGoogle Scholar
  34. 34.
    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nunan N, Wu K, Young IM, Crawford JW, Ritz K (2003) Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil. FEMS Microbiol Ecol 44:203–215CrossRefPubMedGoogle Scholar
  36. 36.
    Hybolt TK, Aamand J, Johnson AR (2011) Quantification of centimetre-scale spatial variation in PAH, glucose and benzoic acid mineralization and soil organic matter in road-side soil. Environ Pollut 159:1085–1091CrossRefGoogle Scholar
  37. 37.
    Grundmann GL (2004) Spatial scales of soil bacterial diversity—the size of a clone. FEMS Microbiol Ecol 48:119–127CrossRefPubMedGoogle Scholar
  38. 38.
    Mummey DL, Clarke JT, Cole CA, O’Connor BG, Gannon JE, Ramsey PW (2010) Spatial analysis reveals differences in soil microbial community interactions between adjacent coniferous forest and clearcut ecosystems. Soil Biol Biochem 42:1138–1147CrossRefGoogle Scholar
  39. 39.
    Kotani-Tanoi T, Nishiyama M, Otsuka S, Senoo K (2007) Single particle analysis reveals that bacterial community structures are semi-specific to the type of soil particle. Soil Sci Plant Nutr 53:740–743CrossRefGoogle Scholar
  40. 40.
    Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290PubMedPubMedCentralGoogle Scholar
  41. 41.
    Philippot L, Bru D, Saby NPA, Cuhel J, Arrouays D, Simek M et al (2009) Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches on the 16S rRNA bacterial tree. Environ Microbiol 11:3096–3104CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Rory Michelland
    • 1
    • 2
    • 3
  • Jean Thioulouse
    • 1
    • 2
    • 4
  • Martina Kyselková
    • 5
  • Genevieve L. Grundmann
    • 1
    • 2
    • 3
    Email author
  1. 1.Université de LyonLyonFrance
  2. 2.Université Lyon 1VilleurbanneFrance
  3. 3.CNRS, UMR5557, Ecologie MicrobienneVilleurbanneFrance
  4. 4.CNRS, UMR5558, Laboratoire de Biométrie et Biologie EvolutiveVilleurbanneFrance
  5. 5.Institute of Soil BiologyBiology Centre of the Czech Academy of SciencesČeské BudějoviceCzech Republic

Personalised recommendations