Seasonal changes of microbial communities in two shallow peat bog lakes

Abstract

Peat bog lakes represent important ecosystems in temperate and boreal zones. We investigated the seasonal dynamics of the microbial community in two small peat bog lakes, Kuźnik Olsowy and Kuźnik Bagienny, located in western Poland. Fluorescence in situ hybridization analyses revealed that the bacterial community was dominated by Proteobacteria and Actinobacteria, in addition to a substantial number of archaea. An infrared epifluorescence analysis demonstrated that aerobic anoxygenic phototrophs (AAPs) constituted a significant fraction of bacterial plankton (1–19 %). All the bacterial groups exhibited large seasonal changes whose course differed between the studied lakes. While chlorophyll had its maximum during winter or early summer, AAPs peaked in summer, when the growth of this group was stimulated by higher irradiance and elevated water temperatures.

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References

  1. Allgaier M, Grossart H-P (2006) Diversity and seasonal dynamics of actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72:3489–3497

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Amann R, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    PubMed Central  CAS  PubMed  Google Scholar 

  3. Andersen R, Chapman SJ, Artz RRE (2013) Microbial communities in natural and disturbed peatlands: a review. Soil Biol Biochem 57:979–994

    Article  CAS  Google Scholar 

  4. Auguet J-C, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4:182–190

    Article  PubMed  Google Scholar 

  5. Auguet J-C, Nomokonova N, Camarero L, Casamayor EO (2011) Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes. Appl Environ Microbiol 77:1974–1945

    Article  Google Scholar 

  6. Basiliko N, Yavitt JB, Dees PM, Merkel SM (2003) Methane biogeochemistry and methanogen communities in two northern peatland ecosystems, New York state. Geomicrobiol J 20:563–577

    Article  CAS  Google Scholar 

  7. Bertoni R, Callieri C, Balseiro E, Modenutti B (2008) Susceptibility of bacterioplankton to nutrient enrichment of oligotrophic and ultraoligotrophic lake waters. J Limnol 67:120–127

    Article  Google Scholar 

  8. Blodau C, Basilico N, Moore TR (2004) Carbon turnover in peatland mesocosm exposed to different water table levels. Biogeochemistry 67:331–351

    Article  CAS  Google Scholar 

  9. Bouvier T, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470

    Article  CAS  Google Scholar 

  10. Burkert UF, Warnecke HD, Babenzien E, Wirnmann Z, Pernthaler J (2003) Members of a readily enriched -proteobacterial clade are common in surface waters of a humic lake. Appl Environ Microbiol 68:6550–6559

    Article  Google Scholar 

  11. Dedysh SN, Panikov NS, Tiedje JM (1998) Acidophilic methanotrophic communities from Sphagnum peat bogs. Appl Environ Microbiol 64:922–9

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Dedysh SN, Pankratov TA, Belova SE, Kulichevskaya IS, Liesack W (2006) Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl Environ Microbiol 72:2110–7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Druvietis I, Springe G, Urtane L, Klavins M (1998) Evaluation of plankton communities in small highly humic bog lakes in Latvia. Environ Int 24:595–602

    Article  CAS  Google Scholar 

  14. Gąbka M, Owsianny PM (2006) Shallow humic lakes of the Wielkopolska region—relation between dystrophy and eutrophy in lake ecosystems. Limnol Rev 6:95–102

    Google Scholar 

  15. Glöckner FO, Fuchs B, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Aquat Microb Ecol 64:1895–1901

    Google Scholar 

  16. Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66:5053–5065

    Article  PubMed Central  PubMed  Google Scholar 

  17. Haukka K, Heikkinen K, Kairesalo T, Karjalainen H, Sivonen K (2005) Effect of humic material on the bacterioplankton community composition in boreal lakes and mesocosms. Environ Microbiol 7:620–630

    Article  CAS  PubMed  Google Scholar 

  18. Hauruseu D, Koblizek M (2012) The influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl Environ Microbiol 78:7414–7419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Høj L, Olsen RA, Torsvik VL (2008) Effects of temperature on the diversity and community structure of known methanogenic groups and other archaea in high Arctic peat. ISME J 2:37–48

    Article  PubMed  Google Scholar 

  20. Hutalle-Schmelzer KML, Elke Zwirnmann E, Angela Kruger A, Grossar H-P (2010) Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. FEMS Microbiol Ecol 72:58–73

    Article  CAS  PubMed  Google Scholar 

  21. Jansson BPM, Malandrin L, Johansson HE (2000) Cell cycle arrest in archaea by the hypusination inhibitor N1-guanyl-1,7-diaminoheptane. J Bacteriol 182:1158–1161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Kirchman D (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microb Ecol 39:91–100

    CAS  Google Scholar 

  23. Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware estuary. Limnol Oceanogr 50:1697–1706

    Article  CAS  Google Scholar 

  24. Klavins M, Rodinv V, Druvietis I (2003) Aquatic chemistry and humic substances in bog lakes in Latvia. Boreal Environ Res 8:113–123

    CAS  Google Scholar 

  25. Koblizek M (2011) Role of photoheterotrophic bacteria in the marine carbon cycle. In: Microbial carbon pump in the ocean, N. Jiao, F. Azam, S. Sanders, eds. Science/AAAS, Washington D.C., pp. 49–51

  26. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495

    Article  CAS  PubMed  Google Scholar 

  27. Kotsyurbenko OR, Chin KJ, Glagolev MV, Stubner S, Simankova MV, Nozhevnikova AN, Conrad R (2004) Acetoclastic and hydrogenotrophic methane production and methanogenic populations in an acidic West-Siberian peat bog. Environ Microbiol 6:1159–1173

    Article  CAS  PubMed  Google Scholar 

  28. Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using Canoco. Cambridge University Press, Cambridge

    Google Scholar 

  29. Lew S, Lew M, Mieszczyński T, Szarek J (2010) Selected fluorescent techniques in analyses of the physiological state of individual water and soil bacterial cells. Folia Microbiol 55:107–118

    Article  CAS  Google Scholar 

  30. Lew S, Lew M, Szarek J, Babińska I (2011) Seasonal patterns of the bacterioplankton community composition in a lake threatened by a pesticide disposal site. Environ Sci Pollut Res 18:376–385

    Article  CAS  Google Scholar 

  31. Lew S, Lew M, Biedunkiewicz A, Szarek J (2013) Impact of pesticide contamination on aquatic microorganism populations in the littoral zone. Arch Environ Contam Toxicol 64:399–409

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Llirós M, Casamayos EO, Borrego C (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol Ecol 66:331–342

    Article  PubMed  Google Scholar 

  33. Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600

    Article  Google Scholar 

  34. Mašín M, Zdun A, Stoń-Egiert J, Nausch M, Labrenz M, Moulisová V, Koblížek M (2006) Seasonal changes and diversity of aerobic anoxygenic phototrophs in the Baltic Sea. Aquat Microbial Ecol 45:247–254

    Article  Google Scholar 

  35. Mašín M, Nedoma J, Pechar L, Koblížek M (2008) Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environ Microbiol 10:1988–1996

    Article  PubMed  Google Scholar 

  36. Mašín M, Čuperová Z, Hojerová E, Salka I, Grossart H-P, Koblížek M (2012) Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquat Microbial Ecol 66:77–86

    Article  Google Scholar 

  37. Newton RJ, Jones SE, Helmus MR, McMahon KD (2007) Phylogenetic ecology of the freshwater actinobacteria acI lineage. Appl Environ Microbiol 73:7169–7176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Pankratov TA, Dedysh SN (2009) Cellulolytic streptomycetes from Sphagnum peat bog and factors controlling their activity. Microbiology 78:227–233

    Article  CAS  Google Scholar 

  39. Pankratov TA, Belova SE, Dedysh SN (2005) Evaluation of the phylogenetic diversity of prokaryotic microorganisms in sphagnum peat bogs by means of fluorescence in situ hybridization (FISH). Microbiology 74:722–728

    Article  CAS  Google Scholar 

  40. Pankratov TA, Dedysh SN, Zavarzin GA (2006) The leading role of actinobacteria in aerobic cellulose degradation in Sphagnum peat bogs. Microbiology 410:428–430

    CAS  Google Scholar 

  41. Pernthaler J, Glöckner FO, Unterholzner S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and archaea in a high mountain lake. Appl Environ Microbiol 64:4299–4306

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Pernthaler A, Pernthaler J, Amann R (2001) Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes (review). Methods Microbiol 30:207–226

    Article  CAS  Google Scholar 

  43. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  44. Preston MD, Smemo KA, McLaughlin JW, Basiliko N (2012) Peatland microbial communities and decomposition processes in the James Bay lowlands Canada. Frontiers Mircobiol 70:1–15

    Google Scholar 

  45. Raghoebarsing AA, Smolders AJ, Schmid MC, Rijpstra WI, Wolters-Arts M, Derksen J, Jetten MS, Schouten S, Sinninghe Damsté JS, Lamers LP, Roelofs JG, Op den Camp HJ, Strous M (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436:1153–115

    Article  CAS  PubMed  Google Scholar 

  46. Roller C, Wagner M, Amann R, Ludwig W, Schleifer KH (1994) In situ probing of Gram-positive bacteria with high DNA G+C content using 23S rRNA-targeted oligonucleotides. Microbiology 140:2849–2858

    Article  CAS  PubMed  Google Scholar 

  47. Šimek K, Babenzien D, Bittl T, Koschel R, Macek M, Nedoma J, Vrba V (1998) Microbial food webs in an artificially divided acidic bog lake. Internat Rev Hydrobiol 83:3–18

    Article  Google Scholar 

  48. Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 205–248

    Google Scholar 

  49. Taipale S, Jones RI, Tiirola M (2009) Vertical diversity of bacteria in an oxygen-stratified humic lake, evaluated using DNA and phospholipid analyses. Aquat Microb Ecol 55:1–16

    Article  Google Scholar 

  50. Taipale S, Kankaala P, Hahn MW, Jones RI, Tiirola M (2011) Methane-oxidizing and photoautotrophic bacteria are major producers in a humic lake with a large anoxic hypolimnion. Aquat Microb Ecol 64:81–95

    Article  Google Scholar 

  51. ter Braak CJF. Šmilauer P (2002) CANOCO reference manual and user’s guide to Canoco for Windows Software for Canonical Community Ordination version 4.5. microcomputer power Ithaca, NY

  52. Tranvik LJ (1998) Degradation of dissolved organic matter in humic waters by bacteria. Ecol Stud 133:259–283

    Article  CAS  Google Scholar 

  53. Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143

    Article  CAS  PubMed  Google Scholar 

  54. Yurkov VV, Csotonyi JT (2009) New light on aerobic anoxygenic phototrophs. In: Daldal F, Thurnauer MC, Beaty JT (eds) Hunter CN. The purple phototrophic bacteria, Springer Verlag, pp 31–55

    Google Scholar 

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Acknowledgment

This study was supported by a grant within scientific investigation project National Center Science (N N305 016940), Algatech (CZ.1.05/2.1.00/03.0110), and GAČR 13-11281S.

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Correspondence to Sylwia Lew.

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Lew, S., Koblížek, M., Lew, M. et al. Seasonal changes of microbial communities in two shallow peat bog lakes. Folia Microbiol 60, 165–175 (2015). https://doi.org/10.1007/s12223-014-0352-0

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Keywords

  • Microbial Community
  • Dissolve Organic Matter
  • Detrended Correspondence Analysis
  • Colored Dissolve Organic Matter
  • Total Bacterium