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Environmental Science and Pollution Research

, Volume 26, Issue 9, pp 9379–9389 | Cite as

Vertical variation of bulk and metabolically active prokaryotic community in sediment of a hypereutrophic freshwater lake

  • Shun TsuboiEmail author
  • Ayato Kohzu
  • Akio Imai
  • Kazuhiro Iwasaki
  • Shigeki YamamuraEmail author
Short Research and Discussion Article
  • 121 Downloads

Abstract

This study was conducted to acquire novel insight into differences between bulk (16S rDNA) and metabolically active (16S rRNA) prokaryotic communities in the sediment of a hypereutrophic lake (Japan). In the bulk communities, the class Deltaproteobacteria and the order Methanomicrobiales were dominant among bacteria and methanogens. In the metabolically active communities, the class Alphaproteobacteria and the order Methanomicrobiales and the family Methanosaetaceae were frequently found among bacteria and methanogens. Unlike the bulk communities of prokaryotes, the composition of the metabolically active communities varied remarkably vertically, and their diversities greatly decreased in the lower 20 cm of sediment. The metabolically active prokaryotic community in the sediment core was divided into three sections based on their similarity: 0–6 cm (section 1), 9–18 cm (section 2), and 21–42 cm (section 3). This sectional distribution was consistent with the vertical pattern of the sedimentary stable carbon and nitrogen isotope ratios and oxidation–reduction potential in the porewater. These results suggest that vertical disturbance of the sediment may influence the communities and functions of metabolically active prokaryotes in freshwater lake sediments. Overall, our results indicate that rRNA analysis may be more effective than rDNA analysis for evaluation of relationships between actual microbial processes and material cycling in lake sediments.

Keywords

Prokaryotic community Freshwater lake Sediment Vertical disturbance 16S rDNA 16S rRNA 

Notes

Acknowledgements

The authors thank the staff at the National Institute for Environmental Studies for collecting sediment samples. The authors also thank Ms. Shigemi Taguchi for assistance with the clone library constructions. We also thank two anonymous reviewers for their constructive comments and suggestions, which helped to improve this paper.

Supplementary material

11356_2019_4465_MOESM1_ESM.pptx (55 kb)
ESM 1 (PPTX 55.4 kb)

References

  1. Aguayo P, González P, Campos V, Maugeri TL, Papale M, Gugliandolo C, Martinez MA (2017) Comparison of prokaryotic diversity in cold, oligotrophic remote lakes of Chilean Patagonia. Curr Microbiol 74:598–613CrossRefGoogle Scholar
  2. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  3. Bai Y, Shi Q, Wen D, Li Z, Jefferson WA, Feng C, Tang X (2012) Bacterial communities in the sediments of Dianchi Lake, a partitioned eutrophic waterbody in China. PLoS One 7:e37796CrossRefGoogle Scholar
  4. Benz M, Schink B, Brune A (1998) Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl Environ Microbiol 64:4507–4512Google Scholar
  5. Chan OC, Claus P, Casper P, Ulrich A, Lueders T, Conrad R (2005) Vertical distribution of structure and function of the methanogenic archaeal community in Lake Dagow sediment. Environ Microbiol 7:1139–1149CrossRefGoogle Scholar
  6. Cheng W, Zhang J, Wang Z, Wang M, Zie S (2014) Bacterial communities in sediments of a drinking water reservoir. Ann Microbiol 64:875–878CrossRefGoogle Scholar
  7. Chernitsyna SM, Mamaeva EV, Lomakina AV, Pogodaeva TV, Galach’yants YP, Bukin SV, Pimenov NV, Khlystov OM, Zemskaya TI (2016) Phylogenetic diversity of microbial communities of the Posolsk Bank bottom sediments, Lake Baikal. Microbiol 85:672–680CrossRefGoogle Scholar
  8. Green PN (2006) Methylobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 257–265CrossRefGoogle Scholar
  9. Green TJ, Barnes AC, Bartkow M, Gale D, Grinham A (2012) Sediment bacteria and archaea community analysis and nutrient fluxes in a sub-tropical polymictic reservoir. Aquat Microb Ecol 65:287–302CrossRefGoogle Scholar
  10. Kamiya K, Fukushima T, Onda Y, Matsushige K, Mizugaki S (2009) Changes in sedimentation rates an phosphorus accumulation in shallow Japanese lakes during 30 years. Verh Internat Verein Limnol 30:1219–1224Google Scholar
  11. Koizumi Y, Kojima H, Fukui M (2003) Characterization of depth-related microbial community structure in lake sediment by denaturing gradient gel electrophoresis of amplified 16S rDNA and reversely transcribed 16S rRNA fragments. FEMS Microbiol Ecol 46:147–157CrossRefGoogle Scholar
  12. Kristensen P, Søndergaard M, Jeppensen E (1992) Resuspension in a shallow eutrophic lake. Hydrobiologia 228:101–109CrossRefGoogle Scholar
  13. Laverock B, Tait K, Gilbert JA, Osborn AM, Widdicombe S (2014) Impacts of bioturbation on temporal variation in bacterial and archaeal nitrogen-cycling gene abundance in coastal sediments. Environ Microbiol Rep 6:113–121CrossRefGoogle Scholar
  14. Li S, Xiao X, Yin X, Wang F (2006) Bacterial community along a historic lake sediment core of Ardley Island, west Antarctica. Extremophiles 10:461–467CrossRefGoogle Scholar
  15. Luna GM, Manini E, Danovaro R (2002) Large fraction of dead and inactive bacteria in coastal marine sediments: comparison of protocols for determination and ecological significance. Appl Environ Microbiol 68:3509–3513CrossRefGoogle Scholar
  16. Miskin IP, Farrimond P, Head IM (1999) Identification of novel bacterial lineages as active members of microbial populations in a freshwater sediment using a rapid RNA extraction procedure and RT-PCR. Microbiol 145:1977–1987CrossRefGoogle Scholar
  17. Nealson KH (1997) Sediment bacteria: who’s there, what are they doing, and what’s new? Annu Rev Earth Planet Sci 25:403–434CrossRefGoogle Scholar
  18. Röske K, Röske I, Uhlmann D (2008) Characterization of the bacterial population and chemistry in the bottom sediment of a laterally subdivided drinking water reservoir system. Limnologica 38:367–377CrossRefGoogle Scholar
  19. Röske K, Sachse R, Scheerer C, Röske I (2012) Microbial diversity and composition of the sediment in the drinking water reservoir Saidenbach (Saxonia, Germany). Syst Appl Microbiol 35:35–44CrossRefGoogle Scholar
  20. Schwarz JIK, Eckert W, Conrad R (2007) Community structure of archaea and bacteria in a profundal lake sediment Lake Kinneret (Israel). Syst Appl Microbiol 30:239–254CrossRefGoogle Scholar
  21. Schwarz JIK, Eckert W, Conrad R (2008) Response of the methanogenic microbial community of a profundal lake sediment (Lake Kinneret, Israel) to algal deposition. Limnol Oceanogr 53:113–121CrossRefGoogle Scholar
  22. Song H, Li Z, Du B, Wang G, Ding Y (2011) Bacterial communities in sediments of the shallow Lake Dongping in China. J Appl Microbiol 112:79–89CrossRefGoogle Scholar
  23. Spring S, Schulze R, Overmann J, Schleifer KH (2000) Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studies. FEMS Microbiol Rev 24:573–590CrossRefGoogle Scholar
  24. Svensson JM (1997) Influence of Chironomus plumosus larvae on ammonium flux and denitrification (measured by the acetylene blockage- and the isotope pairing-technique) in eutrophic lake sediment. Hydrobiologia 346:157–168CrossRefGoogle Scholar
  25. Svensson JM, Enrich-Prast A, Leonardson L (2001) Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquat Microb Ecol 23:177–186CrossRefGoogle Scholar
  26. Tsuboi S, Yamamura S, Imai A, Satou T, Iwasaki K (2014) Linking temporal changes in bacterial community structures with the detection and phylogenetic analysis of neutral metalloprotease genes in the sediments of a hypereutrophic lake. Microbes Environ 29:314–321Google Scholar
  27. Wan Y, Ruan X, Zhang Y, Li R (2017) Illumina sequencing-based analysis of sediment bacteria community in different trophic status freshwater lakes. MicrobiologyOpen 6:e450CrossRefGoogle Scholar
  28. Watanabe T, Kimura M, Asakawa S (2006) Community structure of methanogenic archaea in paddy field soil under double cropping (rice-wheat). Soil Biol Biochem 38:1264–1274CrossRefGoogle Scholar
  29. Xiong W, Xie P, Wang S, Niu Y, Yang X, Chen W (2015) Sources of organic matter affect depth-related microbial community composition in sediments of Lake Erhai, Southwest China. J Limnol 74:310–323Google Scholar
  30. Yang Y, Li N, Wang W, Li B, Xie S, Liu Y (2017) Vertical profiles of sediment methanogenic potential and communities in two freshwater lakes. Biogeosci 14:341–351CrossRefGoogle Scholar
  31. Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, Zhao D (2009) Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol 25:225–233CrossRefGoogle Scholar
  32. Zeng J, Zhao D-Y, Liu P, Yu Z-B, Huang R, Wu QL (2014) Effects of benthic macrofaunal bioturbation on the bacterial community composition in lake sediments. Can J Microbiol 60:517–524CrossRefGoogle Scholar
  33. Zhang J, Yang Y, Zhao L, Li Y, Xie S, Liu Y (2015) Distribution of sediment bacterial and archaeal communities in plateau freshwater lakes. Appl Microbiol Biotechnol 99:3291–3302CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Center for Regional Environmental ResearchNational Institute for Environmental Studies (NIES)TsukubaJapan
  2. 2.Institute for Agro-Environmental SciencesNational Agriculture and Food Research Organization (NARO)TsukubaJapan
  3. 3.Lake Biwa Branch OfficeNational Institute for Environmental Studies (NIES)OtsuJapan

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