The Local Ecological Memory of Soil: Majority and Minority Components of Bacterial Communities in Prehistorical Urns from Schöps (Germany)

Abstract

Soil samples from five iron-age urns and five outside reference samples are investigated by 16S RNA sequencing (ngs) to evaluate the effect of the urns on the soil bacterial diversity. The urns are approximately 2000 years old and had been found during an archaeological excavation of the wet subground of an agricultural used area. All ten samples show similar distribution of phyla. Some major components show differences between the inside-urn and the outside-urn samples. Thus, the interior of urns is marked by a slightly enhanced percentage of Actinobacteria in comparison with the reference samples, whereas no difference between inside-urn samples and reference samples were found in the Chloroflexi content. Between the minor components, some operational taxonomic units (OTUs) could be proved which were found in several urns, but in no reference samples, among them the group TSCOR001-H18 (bacilli), Fodinicola and Angustibacter, NS11-12 marine group and the group S15-21. In addition, several OTUs were detected in single urns, which had been not provable in all other samples. The comparison between the individual urns and between urns and reference samples suggest that the minor components can be regarded as reflecting a signature-like sample-specific soil bacterial DNA pattern, which might become interesting in future investigations on the comparison of archaeological excavation sites and for the registration of bacterial diversity and gene resources at these places.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. Aanderud ZT, Jones SE, Fierer N, Lennon JT (2015) Resuscitation of rare biosphere contributes to pulses of ecosystem activity. Front Microbiol 6:24

    Article  Google Scholar 

  2. An DS, Lee HG, Im WT, Liu OM, Lee ST (2007) Segetibacter koreensis gen. nov., sp nov., a novel member of the phylum bacteriodetes, isolated from the soil of a ginseng field in South Korea. Int J Syst Evol Microbiol 8:1828–1833

    Article  CAS  Google Scholar 

  3. Anantharaman K, Brown CT, Burstein D, Castelle CJ, Probst AJ, Williams KH, Banfield JF (2016) Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum. PEERJ 4:e1607

    Article  CAS  Google Scholar 

  4. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Evol Syst 7:27–49

    Article  Google Scholar 

  5. Bogan BW, Sullivan WR, Kayser KJ, Derr KC, Aldrich HC, Peterek JP (2003) Alkanindiges illinoisensis gen. nov., so nov., an obligately hydrocarbonoclastic, aerobic squalene-degrading bacterium isolated from oilfield soils. Int J Syst Evol Microbiol 53:1389–1395

    Article  CAS  Google Scholar 

  6. Brazelton WJ, Ludwig KA, Sogin ML, Andreishcheva EN, Kelly DS, Shen CC, Edwards RL, Baross JA (2010) Archaea and bacteria with surprising microdiversity show shifts in dominance over 1000-year time scales in hydrothermal chimneys. PNAS 107:1612–1617

    Article  Google Scholar 

  7. Carlsohn MR, Groth I, Saluz HP, Schumann P, Stackebrandt E (2008) Fodinicola feengrottensis gen. nov., sp nov., an actinomycete isolated from a medieval mine. Int J Syst Evol Microbiol 58:1529–1536

    Article  CAS  Google Scholar 

  8. Chen SY, Dong XZ (2005) Proteiniphilum acetatigenes gen. nov., sp. nov., from UASB reactor treating brewery wastewater. Int J Syst Ecol Microbiol 55:2257–2261

    Article  CAS  Google Scholar 

  9. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631

    Article  CAS  Google Scholar 

  10. Fierer N, Lennon JT (2011) The generation and maintenance of diversity in microbial communities. Am J Bot 98:439–448

    Article  Google Scholar 

  11. Fierer N, Bradford MA, Jackson JB (2007) Towards an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  Google Scholar 

  12. Gonella E, Negri I, Marzorati M et al (2011) Bacterial endosymbiont localization in Hyalesthes obsoletus, the insect vector of Bois Noir in Vitis vinifera. Appl Envir Microbiol 77:1423–1435

    Article  CAS  Google Scholar 

  13. Greening RC, Leedle JAZ (1989) Enrichment and isolation of Acetitomaculum ruminis, gen. nov., sp. nov.: acetogenic bacteria from the bovin rumen. Arch Microbiol 151:399–406

    Article  CAS  Google Scholar 

  14. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2001) Using ecological diversity measures with bacterial communities. FEMS Microbiol Evol 43:1–11

    Google Scholar 

  15. Hiraishi A, Shin YK, Sugiyama J (1997) Proposal to reclassify Zoogloea ramigera IAM 12670 (P.R. Dugan 115) as Duganella zoogloeoides gen. nov., sp. nov. Int J Syst Evol Microbiol 47:1249–1252

    CAS  Google Scholar 

  16. Imhoff JF, Labes A, Wiese J (2011) Bio-mining the microbial treasures oft he ocean: new natural products. Biotechn Adv 5:468–482

    Article  CAS  Google Scholar 

  17. Jiao S, Luo YT, Lu MM, Xiao X, Lin YB, Chen WM, Wei GW (2017a) Distinct succession patterns of abundant and rare bacteria in temporal microcosms with pollutants. Environ Pollut 225:497–505

    Article  CAS  Google Scholar 

  18. Jiao S, Zhang ZQ, Yang F, Lin YB, Chen WM, Wei GH (2017b) Temporal dynamics of microbial communities in microcosms in response to pollutants. Mol Ecol 26:923–936

    Article  CAS  Google Scholar 

  19. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. PNAS 107:5881–5886

    Article  Google Scholar 

  20. Kim SB, Lonsdale L, Seong CN, Goodfellow M (2003) Strepacdiphilus gen. nov., acidophilic actinomycetes with wall chemotype I and emendation of the family Streptomacetaceae (Waksman and Henrici (1943)(AL)) emend. Rainey et al. 1997. Antonie Van Leeuwenhoek 83:107–116

    Article  CAS  Google Scholar 

  21. Kim TS, Han JH, Kim SB (2014) Conyzicola lurida gen. nov., sp nov., isolated from the root of Conyza Canadensis. Int J Syst Evol Microbiol 64:2753–2757

    Article  CAS  Google Scholar 

  22. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1

    Article  CAS  Google Scholar 

  23. Kraemer SA, Kassen R (2016) Temporal patterns of local adaptation in soil pseudomonads. Proc R Soc B 283:20161652

    Article  Google Scholar 

  24. Li HR, Yu Y, Luo M, Zeng YX (2010) Marisediminicola Antarctica gen. Nov., sp. Nov., an actinobacterium isolated from the Antarctic. Int J Syst Evol Microbiol 60:2535–2539

    Article  CAS  Google Scholar 

  25. Liao J, Cao X, Wang J, Zhao L, Sun S, Jiang D, Huang Y (2017) Similar community assembly mechanism underlie similar biogeography of rare and abundant bacteria in lakes on Yungui plateau, China. Limnol Oceanogr 62:723–735

    Article  Google Scholar 

  26. Luitjen MLGC, DeWeert J, Smidt H, Boschker HTS, DeVos WM, Schraa G, Stams AJM (2003) Description of Sulfurospirillum halorespirans sp nov., an anaerobic, tetrachloroethene-respiring bacterium, and transfer of Dehalospirillum multivorans to the genus Sulfuspirillum as Sulfuspirillum multivorans comb. nov. Int J Syst Evol Microbiol 53:787–793

    Article  CAS  Google Scholar 

  27. Margesin R, Siles JA, Cajthaml T, Ohlinger B, Kistler E (2017) Microbiology meets archaeology: soil microbial communities reveal different human activities at archaic Monte Iato (sixth century BC). Microbial Ecol 73:925–938

    Article  CAS  Google Scholar 

  28. Maslov S, Sneppen K (2015) Diversity waves in collapse-driven population dynamics. PLoS Comput Biol 11:e1004440

    Article  CAS  Google Scholar 

  29. Nakamura K, Haruta S, Ueno S, Ishii M, Yakota A, Igarashi Y (2004) Cerasibacillus quisquiliarum gen. nov., sp nov., isolated from a semi-continuous decomposing system of kitchen refuce. Int J Syst Evol Microbiol 54:1063–1069

    Article  CAS  Google Scholar 

  30. Nedashkovskaya OI, Kim SB, Han SK, Rhee MS, Lysenko AM, Falsen E, Frolova GM, Mikhailov VV, Bae KS (2004) Ulvibacter litoralis gen. nov., sp nov., a novel member of the Flavobacteriaceae isolated from the green alga Ulva fenestra. Int J Syst Evol Microbiol 54:119–123

    Article  CAS  Google Scholar 

  31. Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356

    Article  Google Scholar 

  32. Prashar P, Kapoor N, Sachdeva S (2014) Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Biotechnol 1:63–77

    Article  CAS  Google Scholar 

  33. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  Google Scholar 

  34. Rezgui R, Abderrazak M, Fardeau ML, Gam ZBA, Cayol JL, Hamed SB, Labat M (2012) Int J Syst Ecol Microbiol 62:2469–2474

    Article  CAS  Google Scholar 

  35. Song J, Choo YJ, Cho JC (2008) Perludicibacter piscinae gen. nov., sp nov., a freshwater bacterium belonging to the family Moraxellaceae. Int J Syst Evol Microbiol 58:97–102

    Article  CAS  Google Scholar 

  36. Soo RM, Woodcroft BJ, Parks DH (2015) Back from the dead: the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus. PEERJ 3:e968

    Article  CAS  Google Scholar 

  37. Tan JQ, Rattray JB, Yang X, Jiang L (2017) Spatial storage effect promotes biodiversity during adaptive radiation. Proc R Soc B Biol Sci 284:20170841

    Article  Google Scholar 

  38. Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    Article  CAS  Google Scholar 

  39. Torsvik V, Sorheim R, Gokskoyr J (1996) Total bacterial diversity in soil and sediment communities—a review. J Ind Microbiol 17:170–178

    CAS  Google Scholar 

  40. Vandamme PA (2016) Proposal of Verticiella gen. nov as replacement for the illegitimate prokaryotic genus name Verticia Vandamme et al. 2015. Int J Syst Evol Microbiol 66:5099–5100

    Article  CAS  Google Scholar 

  41. Vartoukian SR, Downes J, Palmer RM, Wade WG (2013) Fretibacterium fastuosum gen. nov., sp nov., isolated from human oral cavity. Int J Syst Evol Microbiol 63:458–463

    Article  CAS  Google Scholar 

  42. Watanabe T, Kojima H, Fukui M (2015) Sulfuriferual multivorans gen. nov., sp nov., isolated from a freshwater lake, reclassification of ‘Thiobacillus plumbophilus’ as Sulfuriferula plumbophilus sp nov., and description of Sulfuricellaceae fam nov. and Sulfuricellales ord. nov. Int J Syst Evol Microbiol 65:1504–1508

    Article  CAS  Google Scholar 

  43. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glockner FO (2014) The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acid Res 42:D643–D648

    Article  CAS  Google Scholar 

  44. Zhang DC, Redzic M, Schinner F, Margesin R (2011) Glaciimonas immobilis gen. nov., sp nov., a member oft he family Oxalobacteraceae isolated from alpine glacier cryoconite. Int J Syst Evol Microbiol 61:2186–2190

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S-Biomedical (Dr. Bernhard Pätzold) for support for ngs sequencing. The support of SILVA for the data processing is gratefully acknowledged.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Johann Michael Köhler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 22 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Köhler, J.M., Kalensee, F., Günther, P.M. et al. The Local Ecological Memory of Soil: Majority and Minority Components of Bacterial Communities in Prehistorical Urns from Schöps (Germany). Int J Environ Res 12, 575–584 (2018). https://doi.org/10.1007/s41742-018-0116-9

Download citation

Keywords

  • Microbial diversity
  • Soil bacterial communities
  • Prehistoric burials
  • Pre-roman iron age
  • Microorganism signatures