Microbial Ecology

, Volume 63, Issue 3, pp 496–508 | Cite as

Dissolved Organic Carbon as Major Environmental Factor Affecting Bacterioplankton Communities in Mountain Lakes of Eastern Japan

  • Masanori Fujii
  • Hisaya KojimaEmail author
  • Tomoya Iwata
  • Jotaro Urabe
  • Manabu Fukui
Environmental Microbiology


Relationships between environmental factors and bacterial communities were investigated in 41 freshwater lakes located in mountainous regions of eastern Japan. Bacterioplankton community composition (BCC) was determined by polymerase chain reaction-denaturing gradient gel electrophoresis of the 16S rRNA gene and then evaluated on the basis of physicochemical and biological variables of the lakes. Canonical correspondence analysis revealed that BCC of oligotrophic lakes was significantly influenced by dissolved organic carbon (DOC) content, but its effect was not apparent in the analysis covering all lakes including mesotrophic and eutrophic ones. The generalized linear model showed the negative association of DOC on the taxon richness of bacterioplankton communities. DOC was positively correlated with the catchment area per lake volume, suggesting that a large fraction of DOC supplied to the lake was derived from terrestrial sources. These results suggest that allochthonous DOC has a significant effect on bacterioplankton communities especially in oligotrophic lakes. The genus Polynucleobacter was detected most frequently. The occurrence of Polynucleobacter species was positively associated with DOC and negatively associated with total phosphorus (TP) levels. In addition, TP had a stronger effect than DOC, suggesting that oligotrophy is the most important factor on the occurrence of this genus.


Total Phosphorus Canonical Correspondence Analysis Dissolve Organic Carbon Concentration Taxon Richness Freshwater Environment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank T. Hirao for his critical advice and technical assistance in statistical analysis. We also thank T. Suzuki, R. Yagami, K. Hosaka, and K. Suematsu for their field assistance and for providing data of environmental parameters. This study was supported by a grant in aid from the Ministry of Environment for the Global Environment Research Fund (F-052) and was partially supported by a grant from the Ministry of Education, Culture, Sports, Science and Technology, Japan, to Fukui (22370005).

Supplementary material

248_2011_9983_MOESM1_ESM.xls (66 kb)
ESM 1 (XLS 66 kb)


  1. 1.
    de Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758PubMedCrossRefGoogle Scholar
  2. 2.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631PubMedCrossRefGoogle Scholar
  3. 3.
    Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna J, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc Natl Acad Sci USA 104:20404–20409PubMedCrossRefGoogle Scholar
  4. 4.
    Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104:11436–11440PubMedCrossRefGoogle Scholar
  5. 5.
    Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69:2253–2268PubMedCrossRefGoogle Scholar
  6. 6.
    Salcher MM, Pernthaler J, Zeder M, Psenner R, Posch T (2008) Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. Environ Microbiol 10:2074–2086PubMedCrossRefGoogle Scholar
  7. 7.
    Zwart G, Crump BC, Agterveld MPK, Hagen F, Han S (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155CrossRefGoogle Scholar
  8. 8.
    Haukka K, Kolmonen E, Hyder R, Hietala J, Vakkilainen K, Kairesalo T, Haario H, Sivonen K (2006) Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb Ecol 51:137–146PubMedCrossRefGoogle Scholar
  9. 9.
    Lindström ES (2000) Bacterioplankton community composition in five lakes differing in trophic status and humic content. Microb Ecol 40:104–113PubMedGoogle Scholar
  10. 10.
    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 71:8201–8206PubMedCrossRefGoogle Scholar
  11. 11.
    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 72:5478–5485PubMedCrossRefGoogle Scholar
  12. 12.
    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239PubMedCrossRefGoogle Scholar
  13. 13.
    Watson SB, McCauley E, Downing JA (1997) Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnol Oceanogr 42:487–495CrossRefGoogle Scholar
  14. 14.
    Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6:1228–1243PubMedCrossRefGoogle Scholar
  15. 15.
    Sundh I (1992) Biochemical composition of dissolved organic carbon derived from phytoplankton and used by heterotrophic bacteria. Appl Environ Microbiol 58:2938–2947PubMedGoogle Scholar
  16. 16.
    Van der Gucht K, Sabbe K, De Meester L, Vloemans N, Zwart G, Gillis M, Vyverman W (2001) Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ Microbiol 3:680–690CrossRefGoogle Scholar
  17. 17.
    Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  18. 18.
    Tranvik LJ (1992) Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop. Hydrobiologia 229:107–114CrossRefGoogle Scholar
  19. 19.
    Bushaw KL, Zepp RG, Tarr MA, Schulz-Jander D, Bourbonniere RA, Hodson RE, Miller WL, Bronk DA, Moran MA (1996) Photochemical release of biologically available nitrogen from aquatic dissolved organic matter. Nature 381:404–407CrossRefGoogle Scholar
  20. 20.
    Lund V, Hongve D (1994) Ultraviolet irradiated water containing humic substances inhibits bacterial metabolism. War Res 28:1111–1116CrossRefGoogle Scholar
  21. 21.
    Glaeser SP, Grossart HP, Glaeser J (2010) Singlet oxygen, a neglected but important environmental factor: short-term and long-term effects on bacterioplankton composition in a humic lake. Environ Microbiol 12:3124–3136PubMedCrossRefGoogle Scholar
  22. 22.
    Haukka K, Heikkinen E, Kairesalo T, Karjalainen H, Sivonen K (2005) Effect of humic material on the bacterioplankton community composition in boreal lakes and mesocosms. Environ Microbiol 7:620–630PubMedCrossRefGoogle Scholar
  23. 23.
    Jones SE, Newton RJ, McMahon KD (2009) Evidence for structuring of bacterial community composition by organic carbon source in temperate lakes. Environ Microbiol 11:2463–2472PubMedCrossRefGoogle Scholar
  24. 24.
    American Public Health Association (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, WashingtonGoogle Scholar
  25. 25.
    Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. Fisheries Research Board of Canada, OttawaGoogle Scholar
  26. 26.
    Caron DA (1983) Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures. Appl Environ Microbiol 46:491–498PubMedGoogle Scholar
  27. 27.
    Nagata T, Takai K, Kawabata K, Nakanishi M, Urabe J (1996) The trophic transfer via a picoplankton-flagellate-copepod food chain during a picocyanobacterial bloom in Lake Biwa. Arch Hydrobiol 137:145–160Google Scholar
  28. 28.
    Foissner W, Berger H (1996) A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw Biol 35:375–482Google Scholar
  29. 29.
    Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103CrossRefGoogle Scholar
  30. 30.
    Koizumi Y, Kojima H, Oguri K, Kitazato H, Fukui M (2004) Vertical and temporal shifts in microbial communities in the water column and sediment of saline meromictic Lake Kaiike (Japan), as determined by a 16S rDNA-based analysis, and related to physicochemical gradients. Environ Microbiol 6:622–637PubMedCrossRefGoogle Scholar
  31. 31.
    Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172PubMedCrossRefGoogle Scholar
  32. 32.
    Tourlomousis P, Kemsley EK, Ridgway KP, Toscano MJ, Humphrey TJ, Narbad A (2009) PCR-denaturing gradient gel electrophoresis of complex microbial communities: a two-step approach to address the effect of gel-to-gel variation and allow valid comparisons across a large dataset. Microb Ecol 59:776–786PubMedCrossRefGoogle Scholar
  33. 33.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267PubMedCrossRefGoogle Scholar
  34. 34.
    Oksanen J and Blanchet G (2010) Vegan: community ecology package. R package version 1.17-3.
  35. 35.
    Burnham KP, Anderson DR (2002) Model selection and multimodelinference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  36. 36.
    Dobson AJ (1990) An introduction to generalized linear models. Chapman and Hall, LondonGoogle Scholar
  37. 37.
    R Development Core Team (2009) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0,
  38. 38.
    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 66:5053–5065PubMedCrossRefGoogle Scholar
  39. 39.
    Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726PubMedGoogle Scholar
  40. 40.
    Percent SF, Frischer ME, Vescio PA, Duffy EB, Milano V, McLellan M, Stevens BM, Boylen CW, Nierzwicki-Bauer SA (2008) Bacterial community structure of acid-impacted lakes: what controls diversity? Appl Environ Microbiol 74:1856–1868PubMedCrossRefGoogle Scholar
  41. 41.
    Fenchel T, Blackburn TH (1979) Bacteria and mineral cycling. Academic, LondonGoogle Scholar
  42. 42.
    Geller A (1983) Degradability of dissolved organic lake water compounds in cultures of natural bacterial communities. Arch Hydrobiol 99:60–79Google Scholar
  43. 43.
    Eiler A, Beier S, Sawstrom C, Karlsson J, Bertilsson S (2009) High ratio of bacteriochlorophyll biosynthesis genes to chlorophyll biosynthesis genes in bacteria of humic lakes. Appl Environ Microbiol 75:7221–7228PubMedCrossRefGoogle Scholar
  44. 44.
    Stomp M, Huisman J, Stal LJ, Matthijs HCP (2007) Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. ISME J 1:271–282PubMedGoogle Scholar
  45. 45.
    Burkert U, Warnecke F, Babenzien D, Zwirnmann E, Pernthaler J (2003) Members of a readily enriched beta-proteobacterial clade are common in surface waters of a humic lake. Appl Environ Microbiol 69:6550–6559PubMedCrossRefGoogle Scholar
  46. 46.
    Hahn MW (2003) Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl Environ Microbiol 69:5248–5254PubMedCrossRefGoogle Scholar
  47. 47.
    Hahn MW, Pöckl M, Wu QL (2005) Low intraspecific diversity in a Polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 71:4539–4547PubMedCrossRefGoogle Scholar
  48. 48.
    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 Methods 57:379–390PubMedCrossRefGoogle Scholar
  49. 49.
    Watanabe K, Komatsu N, Ishii Y, Negishi M (2009) Effective isolation of bacterioplankton genus Polynucleobacter from freshwater environments grown on photochemically degraded dissolved organic matter. FEMS Microbiol Ecol 67:57–68PubMedCrossRefGoogle Scholar
  50. 50.
    Wu QL, Hahn MW (2006) Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels. FEMS Microbiol Ecol 57:67–79PubMedCrossRefGoogle Scholar
  51. 51.
    Wu QL, Hahn MW (2006) High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ Microbiol 8:1660–1666PubMedCrossRefGoogle Scholar
  52. 52.
    Hutalle-Schmelzer KML, Zwirnmann E, Krüger A, Grossart H (2010) Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. FEMS Microbiol Ecol 72:58–73PubMedCrossRefGoogle Scholar
  53. 53.
    Hutalle-Schmelzer KML, Zwirnmann E, Krüger A, Grossart H (2010) Changes in pelagic bacteria communities due to leaf litter addition. Microb Ecol 60:462–475PubMedCrossRefGoogle Scholar
  54. 54.
    Blom JF, Hornák K, Šimek K, Pernthaler J (2010) Aggregate formation in a freshwater bacterial strain induced by growth state and conspecific chemical cues. Environ Microbiol 12:2486–2495PubMedCrossRefGoogle Scholar
  55. 55.
    Tarao M, Jezbera J, Hahn MW (2009) Involvement of cell surface structures in size-independent grazing resistance of freshwater actinobacteria. Appl Environ Microbiol 75:4720–4726PubMedCrossRefGoogle Scholar
  56. 56.
    Urabe J, Iwata T, Yagami Y, Kato E, Suzuki T, Hino S, Ban S (2011) Within-lake and watershed determinants of carbon dioxide in surface water: a comparative analysis of a variety of lakes in the Japanese Islands. Limnol Oceanogr 56:49–60CrossRefGoogle Scholar
  57. 57.
    Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D, Gille CM, Hodgson JR, Kitchell JF, Kritzberg ES (2005) Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86:2737–2750CrossRefGoogle Scholar
  58. 58.
    Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC, Bade DL, Kritzberg ES, Bastviken D (2004) Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–243PubMedCrossRefGoogle Scholar
  59. 59.
    Ask J, Karlsson J, Persson L, Ask P, Byström P, Jansson M (2009) Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clear-water lakes. Ecology 90:1923–1932PubMedCrossRefGoogle Scholar
  60. 60.
    Berggren M, Ström L, Laudon H, Karlsson J, Jonsson A, Giesler R, Bergström A-K, Jansson M (2010) Lake secondary production fueled by rapid transfer of low molecular weight organic carbon from terrestrial sources to aquatic consumers. Ecol Lett 13:870–880PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Masanori Fujii
    • 1
  • Hisaya Kojima
    • 1
    Email author
  • Tomoya Iwata
    • 2
  • Jotaro Urabe
    • 3
  • Manabu Fukui
    • 1
  1. 1.The Institute of Low Temperature ScienceHokkaido UniversitySapporoJapan
  2. 2.Department of Ecosocial System EngineeringUniversity of YamanashiKofuJapan
  3. 3.Division of Ecology and Evolutionary Biology, School of Life SciencesTohoku UniversitySendaiJapan

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