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The effect of reconstruction works on planktonic bacterial diversity of a unique thermal lake revealed by cultivation, molecular cloning and next generation sequencing

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Abstract

The aim of this study was to gain detailed information about the diversity of planktonic bacterial communities of a worldwide special peat bedded natural thermal spa lake, and to reveal the effect of a lake wall reconstruction work. To compare the efficiency of different methods used for analyzing bacterial diversity, cultivation, molecular cloning and pyrosequencing were applied simultaneously. Despite the almost unchanged physical–chemical parameters and cell count values of lake water, remarkable differences were observed in the planktonic bacterial community structures during and after the reconstruction by all applied microbiological approaches. Rhodobacter sp. was found to be one of the most abundant community members during the works probably due to the sediment stirring effect of the reconstruction. Following the reconstruction higher diversity was detected than during the works by all approaches. Bacterial strains related to species Chryseobacterium and Exiguobacterium, furthermore sequences related to Arcobacter, Gemmobacter and MWH-UniP1 aquatic group were identified in the highest proportion at that time. Although the differences revealed by cultivation based and independent community structures were significant, only minor disparities were found by molecular cloning and next generation sequencing techniques.

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References

  • Allgaier M, Grossart HP (2006) Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microb 72:3489–3497

    Article  CAS  Google Scholar 

  • Buchan A, Collier LS, Neidle EL, Moran MA (2000) Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage. Appl Environ Microb 66:4662–4672

    Article  CAS  Google Scholar 

  • Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    Article  CAS  PubMed  Google Scholar 

  • Chandler DP, Li SM, Spadoni CM, Drake GR, Balkwill DL, Fredrickson JK, Brockman FJ (1997) A molecular comparison of culturable aerobic heterotrophic bacteria and 16S rDNA clones derived from a deep subsurface sediment. FEMS Microbiol Ecol 23:131–144

    Article  CAS  Google Scholar 

  • Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121

    Article  CAS  Google Scholar 

  • Dang H, Lovell CR (2002) Seasonal dynamics of particle-associated and free-living marine Proteobacteria in a salt marsh tidal creek as determined using fluorescence in situ hybridization. Environ Microbiol 4:287–295

    Article  CAS  PubMed  Google Scholar 

  • Do YS, Schmidt TM, Zahn JA, Boyd ES, de la Mora A, DiSpirito AA (2003) Role of Rhodobacter sp. strain PS9, a purple non-sulfur photosynthetic bacterium isolated from an anaerobic swine waste lagoon, in odor remediation. Appl Environ Microbiol 69:1710–1720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckersley K, Dow CS (1980) Rhodopseudomonas blastica sp. nov.: a member of the Rhodospirillaceae. Microbiology 119:465–473

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2014) Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing. Mol Ecol 23:6073–6090

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • González JM, Whitman WB, Hodson RE, Moran MA (1996) Identifying numerically abundant culturable bacteria from complex communities: an example from a lignin enrichment culture. Appl Environ Microbiol 62:4433–4440

    PubMed  PubMed Central  Google Scholar 

  • Hahn MW (2009) Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria. Int J Syst Evol Microbiol 59:112–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW, Stadler P, Wu QL, Pöckl M (2004) The filtration–acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. J Microbiol Method 57:379–390

    Article  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park S-C, Jeo YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2012) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. doi:10.1093/nar/gks808

    PubMed  PubMed Central  Google Scholar 

  • Krett G, Nagymáté Z, Márialigeti K, Borsodi AK (2016) Seasonal and spatial changes of planktonic bacterial communities inhabiting the natural thermal Lake Hévíz, Hungary. Acta Microbiol Imm H 63:115–130

    Article  Google Scholar 

  • Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123

    Article  CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. J Wiley, New Jersey

    Google Scholar 

  • Liao PC, Huang BH, Huang S (2007) Microbial community composition of the Danshui river estuary of Northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microb Ecol 54:497–507

    Article  PubMed  Google Scholar 

  • Lindeman RL (1942) The trophic-dynamic aspect of ecology. Ecology 23:399–417

    Article  Google Scholar 

  • Lindström ES, Kamst-Van Agterveld MP, Zwart G (2005) Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 71:8201–8206

    Article  PubMed  PubMed Central  Google Scholar 

  • McClung CR, Patriquin DG, Davis RE (1983) Campylobacter nitrofigilis sp. nov., a nitrogen-fixing bacterium associated with roots of Spartina alterniflora Loisel. Int J Syst Evol Microbiol 33:605–612

    Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol R 75:14–49

    Article  CAS  Google Scholar 

  • Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643

    Article  PubMed  PubMed Central  Google Scholar 

  • Nuyanzina-Boldareva EN, Kalashnikov AM, Gaisin VA, Sukhacheva MV, Kuznetsov BB, Gorlenko VM (2014) Characterization of a new strain of a purple nonsulfur bacterium from a thermal spring. Microbiology 83:39–46

    Article  CAS  Google Scholar 

  • Pernthaler J, Zöllner E, Warnecke F, Jürgens K (2004) Bloom of filamentous bacteria in a mesotrophic lake: identity and potential controlling mechanism. Appl Environ Microbiol 70:6272–6281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poindexter JS (2006) Dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 72–90

    Chapter  Google Scholar 

  • Porter ML, Engel AS, Kane TC, Kinkle BK (2009) Productivity–diversity relationships from chemolithoautotrophically based sulfidic karst systems. Int J Speleol 38:4

    Article  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Samarajeewa AD, Hammad A, Masson L, Khan IUH, Scroggins R, Beaudette LA (2015) Comparative assessment of next-generation sequencing, denaturing gradient gel electrophoresis, clonal restriction fragment length polymorphism and cloning-sequencing as methods for characterizing commercial microbial consortia. J Microbiol Method 108:103–111

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Coldspring-Harbour Laboratory Press, UK

    Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semrau JD, DiSpirito AA, Murrell JC (2008) Life in the extreme: thermoacidophilic methanotrophy. Trends Microbiol 16:190–193

    Article  CAS  PubMed  Google Scholar 

  • Sheu SY, Shiau YW, Wei YT, Chen WM (2013) Gemmobacter lanyuensis sp. nov., isolated from a freshwater spring. Int J Syst Evol Microbiol 63:4039–4045

    Article  CAS  PubMed  Google Scholar 

  • Stancheva R, Sheath RG, Read BA, McArthur KD, Schroepfer C, Kociolek JP, Fetscher AE (2013) Nitrogen-fixing cyanobacteria (free-living and diatom endosymbionts): their use in southern California stream bioassessment. Hydrobiologia 720:111–127

    Article  CAS  Google Scholar 

  • Suzuki MT, Rappe MS, Haimberger ZW, Winfield H, Adair N, Ströbel J, Giovannoni SJ (1997) Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample. Appl Environ Microbiol 63:983–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang X, Gao G, Qin B, Zhu L, Chao J, Wang J, Yang G (2009) Characterization of bacterial communities associated with organic aggregates in a large, shallow, eutrophic freshwater lake (Lake Taihu, China). Microb Ecol 58:307–322

    Article  CAS  PubMed  Google Scholar 

  • Tarhriz V, Thiel V, Nematzadeh G, Hejazi MA, Imhoff JF, Hejazi MS (2013) Tabrizicola aquatica gen. nov. sp. nov., a novel alphaproteobacterium isolated from Qurugöl Lake nearby Tabriz city, Iran. Van Leeuw J Microb 104:1205–1215

    Article  CAS  Google Scholar 

  • Tindall BJ, Rosselló-Mora R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    Article  CAS  PubMed  Google Scholar 

  • Tytgat B, Verleyen E, Obbels D, Peeters K, De Wever A, D’hondt S, De Meyer T, Van Criekinge W, Vyverman W, A A (2014) Bacterial diversity assessment in Antarctic terrestrial and aquatic microbial mats: a comparison between bidirectional pyrosequencing and cultivation. PLoS ONE 9:e97564

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaz-Moreira I, Egas C, Nunes OC, Manaia CM (2011) Culture-dependent and culture-independent diversity surveys target different bacteria: a case study in a freshwater sample. Van Leeuw J Microb 100:245–257

    Article  Google Scholar 

  • Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253

    Article  CAS  PubMed  Google Scholar 

  • Williamson CE, Dodds W, Kratz TK, Palmer MA (2008) Lakes and streams as sentinels of environmental change in terrestrial and atmospheric processes. Front Ecol Environ 6:247–254

    Article  Google Scholar 

  • Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad ATLT, Taylor LT, DeLong EF, Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68:316–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QL, Zwart G, Schauer M, Kamst-van Agterveld MP, Hahn MW (2006) Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol 72:5478–5485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QL, Zwart G, Wu J, Kamst-van Agterveld MP, Liu S, Hahn MW (2007) Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environ Microbiol 9:2765–2774

    Article  CAS  PubMed  Google Scholar 

  • Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS (2009) Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 75:5227–5236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Microbiology, Eötvös Loránd University, Pázmány P. sétány 1/C, 1117, Budapest, Hungary

    Gergely Krett, Attila Szabó, Tamás Felföldi, Károly Márialigeti & Andrea K. Borsodi

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  1. Gergely Krett
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  2. Attila Szabó
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  3. Tamás Felföldi
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  4. Károly Márialigeti
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  5. Andrea K. Borsodi
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Correspondence to Andrea K. Borsodi.

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Communicated by Shuang-Jiang Liu.

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Krett, G., Szabó, A., Felföldi, T. et al. The effect of reconstruction works on planktonic bacterial diversity of a unique thermal lake revealed by cultivation, molecular cloning and next generation sequencing. Arch Microbiol 199, 1077–1089 (2017). https://doi.org/10.1007/s00203-017-1379-9

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  • DOI: https://doi.org/10.1007/s00203-017-1379-9

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