Skip to main content
SpringerLink
Log in

IncP-1 and PromA Group Plasmids Are Major Providers of Horizontal Gene Transfer Capacities Across Bacteria in the Mycosphere of Different Soil Fungi

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Plasmids of the IncP-1β group have been found to be important carriers of accessory genes that enhance the ecological fitness of bacteria, whereas plasmids of the PromA group are key agents of horizontal gene transfer in particular soil settings. However, there is still a paucity of knowledge with respect to the diversity, abundance, and involvement in horizontal gene transfer of plasmids of both groups in the mycosphere. Using triparental exogenous isolation based on the IncQ tracer plasmid pSUP104 as well as direct molecular detection, we analyzed the pool of mobilizer and self-transferable plasmids in mycosphere soil. Replicate mushroom types that were related to Russula, Inocybe, Ampulloclitocybe, and Galerina spp. were sampled from a forest soil area, and bulk soil was used as the control. The data showed that the levels of IncP-1β plasmids are significantly raised across several of the mycospheres analyzed, whereas those of PromA group plasmids were similar across the mycospheres and corresponding bulk soil. Moreover, the frequencies of triparental exogenous isolation of mobilizer plasmids into a Pseudomonas fluorescens recipient strain were significantly elevated in communities from several mycospheres as compared with those from bulk soil. Molecular analysis of selected transconjugants, as well as from directly isolated strains, revealed the presence of plasmids of three size groups, i.e., (1) 40–45, (2) 50–60, and (3) ≥60 kb, across all isolations. Replicon typing using IncN, IncW and IncA/C proxies revealed no positive signals. In contrast, a suite of plasmids produced signals with IncP-1β as well as PromA type replicon typing systems. Moreover, a selected subset of plasmids, obtained from the Inocybe and Galerina isolates, was transferred out further, revealing their capacities to transfer and mobilize across a broad host range.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Alvarado A, Garcillán-Barcia MP, de la Cruz F (2012) A degenerate primer MOB typing (DPMT) method to classify Gamma-proteobacterial plasmids in clinical and environmental settings. PLoS ONE 7(7):e40438

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Atkinson GF (1918) Some new species of Inocybe. Am J Bot 5(4):210–218

    Article  Google Scholar 

  3. Bach HJ et al (2002) Enumeration of total bacteria and bacteria with genes for proteolytic activity in pure cultures and in environmental samples by quantitative PCR mediated amplification. J Microbiol Meth 49:235–245

    Article  CAS  Google Scholar 

  4. Bale MJ et al (1988) Novel method for studying plasmid transfer in undisturbed river epilithon. Appl Environ Microbiol 54:2756–2758

  5. Bergstrom CT, Llipsitch M, Levin BR (2000) National selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505–1519

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Boersma FGH (2009) Mechanisms of bacterial selection in the mycosphere of tricholomataceous fungi. PhD Thesis University of Groningen

  8. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  9. Dennis JJ (2005) The evolution of IncP catabolic plasmids. Curr Opin Biotechnol 16:291–298

    Article  CAS  PubMed  Google Scholar 

  10. Earle FS (1909) The genera of North American gill fungi. Bull N Y Bot Gard 5:373–451

    Google Scholar 

  11. Folman LB et al (2008) Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil. FEMS Microbiol Ecol 63:181–191

    Article  CAS  PubMed  Google Scholar 

  12. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732

    Article  CAS  PubMed  Google Scholar 

  13. Götz A et al (1996) Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl Environ Microbiol 62:2621–2628

  14. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  15. Heuer H, Smalla K (2012) Plasmids foster diversification and adaptation of bacterial populations in soil. FEMS Microbiol Rev 36:1083–1104

  16. Mela F et al (2008) Comparative genomics of the pIPO2/pSB102 family of environmental plasmids: sequence, evolution, and ecology of pTer331 isolated from Collimonas fungivorans Ter331. FEMS Microbiol Ecol 66:45–62

    Article  CAS  PubMed  Google Scholar 

  17. Melzer A, Zvára A (1927) Russula exalbicans (Pers.). Arch Prírodov Výzk Cech 17(4):97

    Google Scholar 

  18. Redhead SA, Lutzoni F, Moncalvo JM, Vilgalys R (2002) Phylogeny of agarics: partial systematics solutions for core omphalinoid genera in the Agaricales (euagarics). Mycotaxon 83:19–57

    Google Scholar 

  19. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  20. Sarand I, Haario H, Jörgensen KS, Romantschuk M (2000) Effect of inoculation of a TOL plasmid containing mycorrhizosphere bacterium on development of Scots pine seedlings, their mycorrhizosphere and the microbial flora in m-toluate-amended soil. FEMS Microbiol Ecol 31:127–141

    Article  CAS  PubMed  Google Scholar 

  21. Schlüter A, Szczepanowski R, Pühler A, Top EM (2007) Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol Rev 31:449–477

    Article  PubMed  Google Scholar 

  22. Smalla K, Heuer H, Götz A, Niemeyer D, Krögerrecklenfort E, Tietze E (2000) Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-like plasmids. Appl Environ Microbiol 66:4854–4862

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Smit E et al (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2612–2621

  24. Sota M, Top EM (2008) Horizontal gene transfer mediated by plasmids. In: Lipps G (ed) Plasmids: current research and future trends. Caister Academic Press, Norfolk, UK, pp 111–181

    Google Scholar 

  25. Tauch A, Schneiker S, Selbitschka W, Puhler A, Van Overbeek LS, Smalla K (2002) The complete nucleotide sequence and environmental distribution of the cryptic, conjugative, broad-host-range plasmid pIPO2 isolated from bacteria of the wheat rhizosphere. Microbiology 148:1637–1653

    CAS  PubMed  Google Scholar 

  26. Thomas CM (2000) The horizontal gene pool: bacterial plasmids and gene spread. Harwood Academic Publishers, Amsterdam

    Book  Google Scholar 

  27. Valášková V et al (2009) Phylogenetic composition and properties of bacteria coexisting with the fungus Hypholoma fasciculare in decaying wood. ISME J 3:1218–1221

    Article  PubMed  Google Scholar 

  28. Van der Auwera GA et al (2009) Plasmids captured in C. metallidurans CH34: defining the PromA family of broad-host-range plasmids. Antonie van Leeuwenhoek 96:193–204

  29. Van Elsas JD, Gardener BBM, Wolters AC, Smit E (1998) Isolation, characterization, and transfer of cryptic genemobilizing plasmids in the wheat rhizosphere. Appl Environ Microbiol 64:880–889

    PubMed Central  PubMed  Google Scholar 

  30. Van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol 157:525–537

    Article  Google Scholar 

  31. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  32. Warmink JA, van Elsas JD (2008) Selection of bacterial populations in the mycosphere of Laccaria proxima: is type III secretion involved? ISME J 2:887–900

    Article  CAS  PubMed  Google Scholar 

  33. Warmink JA, Nazir R, van Elsas JD (2009) Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi. Environ Microbiol 11:300–312

    Article  CAS  PubMed  Google Scholar 

  34. Zhang M, Pereira e Silva MC, Chaib de Mares M, van Elsas JD (2014) The mycosphere constitutes an arena for horizontal gene transfer with strong evolutionary implications for bacterial–fungal interactions. FEMS Microbiol Ecol. doi: 10.1111/1574-6941.12350

Download references

Acknowledgments

We thank the CSC funding agency of China for providing support to Miaozhi Zhang. We also thank Jan Warmink, Kexin Zhang, and Aron te Winkel for their assistance in the lab.

Author information

Authors and Affiliations

  1. Department of Microbial Ecology, Center for Ecological and Evolutionary Studies, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands

    Miaozhi Zhang, Sander Visser & Jan Dirk van Elsas

  2. Department of Soil Science, “Luiz de Queiroz” College of Agriculture, University of São Paulo, Av Pádua Dias, 11, 13418-900, Piracicaba, SP, Brazil

    Michele C Pereira e Silva

  3. Department of Microbial Ecology, Centre for Life Sciences, University of Groningen, P.O. BOX 11103, 9700 CC, Groningen, The Netherlands

    Jan Dirk van Elsas

Authors
  1. Miaozhi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sander Visser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michele C Pereira e Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan Dirk van Elsas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jan Dirk van Elsas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(DOCX 33 kb)

Supplementary Table 2

(DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Visser, S., Pereira e Silva, M. et al. IncP-1 and PromA Group Plasmids Are Major Providers of Horizontal Gene Transfer Capacities Across Bacteria in the Mycosphere of Different Soil Fungi. Microb Ecol 69, 169–179 (2015). https://doi.org/10.1007/s00248-014-0482-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0482-6

Keywords

Search

Navigation