Skip to main content
SpringerLink
Log in

Selection of associated heterotrophs by methane-oxidizing bacteria at different copper concentrations

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Due to the increasing atmospheric concentration of the greenhouse gas methane, more knowledge is needed on the management of methanotrophic communities. While most studies have focused on the characteristics of the methane-oxidizing bacteria (MOB), less is known about their interactions with the associated heterotrophs. Interpretative tools based on denaturing gradient gel electrophoresis allowed to evaluate the influence of copper—an important enzymatic regulator for MOB—on the activity and composition of the bacterial community. Over 30 days, enrichments with 0.1, 1.0 and 10 μM Cu2+ respectively, showed comparable methane oxidation activities. The different copper concentrations did not create major shifts in the methanotrophic communities, as a Methylomonas sp. was able to establish dominance at all different copper concentrations by switching between both known methane monooxygenases. The associated heterotrophic communities showed continuous shifts, but over time all cultures evolved to a comparable composition, independent of the copper concentration. This indicates that the MOB selected for certain heterotrophs, possibly fulfilling vital processes such as removal of toxic compounds. The presence of a large heterotrophic food web indirectly depending on methane as sole carbon and energy source was confirmed by a clone library wherein MOB only formed a minority of the identified species.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Balasubramanian R, Rosenzweig AC (2008) Copper methanobactin: a molecule whose time has come. Curr Opin Chem Biol 12(2):245–249. doi:10.1016/J.Cbpa.2008.01.043

    Article  PubMed  CAS  Google Scholar 

  • Bernardet J, Bowman JP (2007) Prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, vol 7. Springer, New York, pp 481–531

    Google Scholar 

  • Boon N, Pycke BFG, Marzorati M, Hammes F (2011) Nutrient gradients in a granular activated carbon biofilter drives bacterial community organization and dynamics. Water Res 45(19):6355–6361. doi:10.1016/J.Watres.2011.09.016

    Article  PubMed  CAS  Google Scholar 

  • Bowman JP (2007) The methanotrophs—the families Methylococcaceae and Methylocystacea. In: The prokaryotes: a handbook on the biology of bacteria, vol 5. Springer, New York, pp 266–289

  • Brusseau GA, Tsien HC, Hanson RS, Wackett LP (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1(1):19–29. doi:10.1007/BF00117048

    Article  PubMed  CAS  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65(11):5066–5074. doi:10.1111/j.1574-6941.2006.00122.x

    PubMed  CAS  Google Scholar 

  • Dalton H (2005) The Leeuwenhoek lecture 2000—The natural and unnatural history of methane-oxidizing bacteria. Philos Trans R Soc Lond Ser B 360(1458):1207–1222. doi:10.1098/Rstb.2005.1657

    Article  CAS  Google Scholar 

  • Dedysh SN (2009) Exploring methanotroph diversity in acidic northern wetlands: molecular and cultivation-based studies. Microbiology 78(6):655–669. doi:10.1134/S0026261709060010

    Article  CAS  Google Scholar 

  • Dunfield PF, Khmelenina VN, Suzina NE, Trotsenko YA, Dedysh SN (2003) Methylocella silvestris sp. nov., a novel methanotroph isolated from an acidic forest cambisol. Int J Syst Environ Microbiol 53:1231–1239. doi:10.1099/Ijs.0.02481-0

    Article  CAS  Google Scholar 

  • Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJCT, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs K-J, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464(7288):543–548. doi:10.1038/nature08883

    Article  PubMed  CAS  Google Scholar 

  • Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241. doi:10.1146/Annurev.Biochem.76.061505.175355

    Article  PubMed  CAS  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60(2):439–471. doi:0146-0749/96/$04.0010

    PubMed  CAS  Google Scholar 

  • Hesselsoe M, Boysen S, Iversen N, Jorgensen L, Murrell JC, McDonald I, Radajewski S, Thestrup H, Roslev P (2005) Degradation of organic pollutants by methane grown microbial consortia. Biodegradation 16(5):435–448. doi:10.1007/s10532-004-4721-2

    Article  PubMed  CAS  Google Scholar 

  • Hoefman S, van der Ha D, De Vos P, Boon N, Heylen K (2012) Miniaturized extinction culturing is the preferred strategy for rapid isolation of fast-growing methane-oxidizing bacteria. Microb Biotechnol 5(3):368–378. doi:10.1111/j.1751-7915.2011.00314.x

    Article  PubMed  CAS  Google Scholar 

  • Hrsak D, Begonja A (2000) Possible interactions within a methanotrophic-heterotrophic groundwater community able to transform linear alkylbenzenesulfonates. Appl Environ Microbiol 66(10):4433–4439. doi:10/1998;85(3):448-56

    Article  PubMed  CAS  Google Scholar 

  • Iguchi H, Yurimoto H, Sakai Y (2011) Stimulation of methanotrophic growth in cocultures by cobalamin excreted by rhizobia. Appl Environ Microbiol 77(24):8509–8515. doi:10.1128/Aem.05834-11

    Article  PubMed  CAS  Google Scholar 

  • Jiang H, Chen Y, Jiang P, Zhang C, Smith TJ, Murrell JC, Xing X-H (2010) Methanotrophs: multifunctional bacteria with promising applications in environmental bioengineering. Biochem Eng J 49(3):277–288. doi:10.1016/j.bej.2010.01.003

    Article  CAS  Google Scholar 

  • Koh SC, Bowman JP, Sayler GS (1993) Soluble methane monooxygenase production and trichloroethylene degradation by a Type-I methanotroph, Methylomonas methanica-68-1. Appl Environ Microbiol 59(4):960–967. doi:0099-2240/93/040960-08$02.00/0

    PubMed  CAS  Google Scholar 

  • Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10(6):1571–1581. doi:10.1111/j.1462-2920.2008.01572.x

    Article  PubMed  CAS  Google Scholar 

  • Melse RW, Van der Werf AW (2005) Biofiltration for mitigation of methane emission from animal husbandry. Environ Sci Technol 39(14):5460–5468. doi:10.1021/Es048048q

    Article  PubMed  CAS  Google Scholar 

  • Modin O, Fukushi K, Nakajima F, Yamamoto K (2010) Aerobic methane oxidation coupled to denitrification: kinetics and effect of oxygen supply. J Environ Eng ASCE 136(2):211–219. doi:10.1061/(Asce)Ee.1943-7870.0000134

    Article  CAS  Google Scholar 

  • Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S, Jetten MSM, Birkeland N-K, Pol A, Dunfield PF (2009) Environmental, genomic and taxonomic perspectives on methanotrophic verrucomicrobia. Environ Microbiol Rep 1(5):293–306. doi:10.1111/j.1758-2229.2009.00022.x

    Article  CAS  Google Scholar 

  • Ovreas L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic lake saelevannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373. doi:0099-2240/97/$04.00+0

    PubMed  CAS  Google Scholar 

  • Read S, Marzorati M, Guimaraes BCM, Boon N (2011) Microbial resource management revisited: successful parameters and new concepts. Appl Microbiol Biotechnol 90(3):861–871. doi:10.1007/S00253-011-3223-5

    Article  PubMed  CAS  Google Scholar 

  • Schrader J, Schilling M, Holtmann D, Sell D, Filho MV, Marx A, Vorholt JA (2008) Methanol-based industrial biotechnology: current status and future perspectives of methylotrophic bacteria. Trends Biotechnol 27(2):107–115. doi:10.1016/j.tibtech.2008.10.009

    Article  PubMed  Google Scholar 

  • Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531. doi:10.1111/j.1574-6976.2010.00212.x

    PubMed  CAS  Google Scholar 

  • van der Ha D, Hoefman S, Boeckx P, Verstraete W, Boon N (2010) Copper enhances the activity and salt resistance of mixed methane-oxidizing communities. Appl Microbiol Biotechnol 87:2355–2363. doi:10.1007/s00253-010-2702-4

    Article  PubMed  Google Scholar 

  • Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang LX, Scanlan D, Kang KH, Lewis M, Nelson KE, Methe B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren QH, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2(10):1616–1628. doi:10.1371/journal.pbio.0020303

    Article  CAS  Google Scholar 

  • Wittebolle L, Vervaeren H, Verstraete W, Boon N (2008) Quantifying community dynamics of nitrifiers in functionally stable reactors. Appl Environ Microbiol 74(1):286–293. doi:10.1128/Aem.01006-07

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors like to thank Tim Lacoere for his assistance during the analyses. This research was funded by a PhD grant for David van der Ha from the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen, SB-83259) and research grants from the Geconcerteerde Onderzoeksactie (GOA) of Ghent University (BOF09/GOA/005) and from the Flemish Fund for Scientific Research (FWO-Vlaanderen, 3G070010).

Conflict of interest

There is no conflict of interest amongst the authors. DVDH and IV contributed equally in the study. SV assisted with the molecular analyses while PDV and NB helped with the design of the study and the manuscript drafting.

Author information

Authors and Affiliations

  1. Laboratory of Microbial Ecology and Technology (LabMET), Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    David van der Ha, Inka Vanwonterghem & Nico Boon

  2. Laboratory of Microbiology, Department of Biochemistry and Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Sven Hoefman & Paul De Vos

  3. BCCM/LMG Culture Collection, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Paul De Vos

Authors
  1. David van der Ha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Inka Vanwonterghem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sven Hoefman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul De Vos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nico Boon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nico Boon.

Additional information

David van der Ha and Inka Vanwonterghem contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 1522 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Ha, D., Vanwonterghem, I., Hoefman, S. et al. Selection of associated heterotrophs by methane-oxidizing bacteria at different copper concentrations. Antonie van Leeuwenhoek 103, 527–537 (2013). https://doi.org/10.1007/s10482-012-9835-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-012-9835-7

Keywords

Search

Navigation