Skip to main content

Advertisement

SpringerLink
Log in

Variations in Bacterial Community in a Temperate Lake Associated with an Agricultural Watershed

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Terrestrially derived carbon and nutrients are washed into lakes, providing nutritional drivers for both microbial heterotrophy and phototrophy. Changes in the quantity and diversity of carbon and nutrients exported from watersheds in response to alterations in long-term land use have led to a need for evaluation of the linkage between watershed-exported carbon and nutrients and bacterial community structure in watershed associated lakes. To learn more about these interactions, we investigated Muskrat Lake in Michigan, which has a well-defined moderately sized watershed dominated by agriculture. We measured the water chemistry, characterized the dissolved organic carbon, and determined the structure of the bacterial communities at the inlet and center of this lake (five depths per site) over the summer and fall of 2008. The lake had temporal and rain event-based fluctuations in water chemistry, as well as temporal and rain event-dependent shifts in bacterial communities as measured by terminal restriction fragment length polymorphism. Agricultural watershed inputs were observed in the lake during and after rain events. Terminal restriction fragment length polymorphism and 454 pyrosequencing of the bacterial communities indicated that there were differences over time and that the dominant phylotypes shifted between summer and late fall. Some populations (e.g., Polynucleobacter and Mycobacterium) increased during fall, while others (e.g., Gemmatimonas) diminished. Redundancy and partitioning analyses showed that water chemistry is highly correlated with variations in the bacterial community of the lake, which explained 34 % of the variations in the bacterial community. Dissolved organic carbon had the greatest effects on variations in the Muskrat Lake bacterial community (2 %). The results of this study provide information that will enable a better understanding of the interaction between the bacterial community of lakes and changes in chemical properties as a result of nutrient importation from the surrounding watershed.

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

  1. Lindström ES (2000) Bacterioplankton community composition in five lakes differing in trophic status and humic content. Microb Ecol 40:104–113

    PubMed  Google Scholar 

  2. Lindström ES (2001) Investigating influential factors on bacterioplankton community composition: results from a field study of five mesotrophic lakes. Microb Ecol 42:598–605

    Article  PubMed  Google Scholar 

  3. 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 74:1856–1868. doi:10.1128/aem.01719-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Reinthaler T, Winter C, Herndl GJ (2005) Relationship between bacterioplankton richness, respiration, and production in the southern North Sea. Appl Environ Microbiol 71:2260–2266. doi:10.1128/aem.71.5.2260-2266.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Schauer M, Hahn MW (2005) Diversity and phylogenetic affiliations of morphologically conspicuous large filamentous bacteria occurring in the pelagic zones of a broad spectrum of freshwater habitats. Appl Environ Microbiol 71:1931–1940. doi:10.1128/aem.71.4.1931-1940.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yannarell AC, Triplett EW (2004) Within- and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales. Appl Environ Microbiol 70:214–223. doi:10.1128/aem.70.1.214-223.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lindström ES, Leskinen E (2002) Do neighboring lakes share common taxa of bacterioplankton? Comparison of 16S rDNA fingerprints and sequences from three geographic regions. Microb Ecol 44:1–9

    Article  PubMed  Google Scholar 

  8. Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna JM, 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 U S A 104:20404–20409

    Article  PubMed  PubMed Central  Google Scholar 

  9. Stepanauskas R, Moran MA, Bergamaschi BA, Hollibaugh JT (2003) Covariance of bacterioplankton composition and environmental variables in a temperate delta system. Aquat Microb Ecol 31:85–98

    Article  Google Scholar 

  10. Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. doi:10.1128/aem.71.1.227-239.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jardillier L, Basset M, Domaizon I, Belan A, Amblard C, Richardot M, Debroas D (2004) Bottom-up and top-down control of bacterial community composition in the euphotic zone of a reservoir. Aquat Microb Ecol 35:259–273

    Article  Google Scholar 

  12. Hullar MAJ, Kaplan LA, Stahl DA (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72:713–722. doi:10.1128/aem.72.1.713-722.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jarone P, Farooq A, Johanna H, Richard AL, Josefina M, Ulla Li Z, Ãke H (1999) Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat Microb Ecol 17:13–26. doi:10.3354/ame017013

    Article  Google Scholar 

  14. Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47

    Article  CAS  PubMed  Google Scholar 

  15. Tranvik LJ (1988) Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb Ecol 16:311–322

    Article  CAS  PubMed  Google Scholar 

  16. van Hannen EJ, Mooij WM, van Agterveld MP, Gons HJ, Laanbroek HJ (1999) Detritus-dependent development of the microbial community in an experimental system: qualitative analysis by denaturing gradient gel electrophoresis. Appl Environ Microbiol 65:2478–2484

    PubMed  PubMed Central  Google Scholar 

  17. Kritzberg ES, Cole JJ, Pace ML, Granéli W, Bade DL (2004) Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnol Oceanogr 49:588–596. doi:10.2307/3597867

    Article  CAS  Google Scholar 

  18. Kritzberg ES, Langenheder S, Lindström ES (2006) Influence of dissolved organic matter source on lake bacterioplankton structure and function—implications for seasonal dynamics of community composition. FEMS Microbiol Ecol 56:406–417. doi:10.1111/j.1574-6941.2006.00084.x

    Article  CAS  PubMed  Google Scholar 

  19. Arbuckle KE, Downing JA (2001) The influence of watershed land use on lake N: P in a predominantly agricultural landscape. Limnol Oceanogr 46:970–975

    Article  Google Scholar 

  20. Gao C, Zhu J, Zhu J, Gao X, Dou Y, Hosen Y (2004) Nitrogen export from an agriculture watershed in the Taihu Lake area, China. Environ Geochem Health 26:199–207

    Article  CAS  PubMed  Google Scholar 

  21. del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Article  Google Scholar 

  22. Dillon PJ, Molot LA (1997) Dissolved organic and inorganic carbon mass balances in central Ontario lakes. Biogeochemistry 36:29–42

    Article  CAS  Google Scholar 

  23. Jordan P, Rippey B, Anderson NJ (2002) The 20th century whole-basin trophic history of an inter-drumlin lake in an agricultural catchment. Sci Total Environ 297:161–173

    Article  CAS  PubMed  Google Scholar 

  24. Kahlert M, Hasselrot AT, Hillebrand H, Pettersson K (2002) Spatial and temporal variation in the biomass and nutrient status of epilithic algae in Lake Erken, Sweden. Freshw Biol 47:1191–1215

    Article  CAS  Google Scholar 

  25. Hessen DO, Andersen T, Lyche A (1990) Carbon metabolism in a humic lake—pool sizes and cycling through zooplankton. Limnol Oceanogr 35:84–99

    Article  CAS  Google Scholar 

  26. Lennon JT, Pfaff LE (2005) Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquat Microb Ecol 39:107–119

    Article  Google Scholar 

  27. Song L, Marsh TL, Voice TC, Long DT (2011) Loss of seasonal variability in a lake resulting from copper sulfate algaecide treatment. Phys Chem Earth Parts A/B/C 36:430–435

    Article  Google Scholar 

  28. MSU (2009) Michigan State University, Horticulture Teaching and Research Center, Michigan Automated Weather Network. http://www.agweather.geo.msu.edu/mawn/station.asp?id=msu. Accessed June 2009

  29. APHA (1998) Standard Methods for the Evaluation of Water and Wastewater. American Public Health Association Publishing. Washington, DC

    Google Scholar 

  30. Chin Y-P, Aiken G, O’Loughlin E (1994) Molecular weight, polydispersity, and spectroscopic properties of aquatic humic substances. Environ Sci Technol 28:1853–1858

    Article  CAS  PubMed  Google Scholar 

  31. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  CAS  PubMed  Google Scholar 

  33. Hopkinson CS, Buffam I, Hobbie J, Vallino J, Perdue M, Eversmeyer B, Prahl F, Covert J, Hodson R, Moran MA, Smith E, Baross J, Crump B, Findlay S, Foreman K (1998) Terrestrial inputs of organic matter to coastal ecosystems: an intercomparison of chemical characteristics and bioavailability. Biogeochemistry 43:211–234

    Article  CAS  Google Scholar 

  34. Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  35. Hammer Ø, Harper, D.A.T., and P. D. Ryan (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4 (1): 9. doi: http://palaeo-electronica.org/2001_1/past/issue1_01.htm

  36. Hill MO, Gauch HG (1980) Detrended correspondence analysis—an improved ordination technique. Vegetatio 42:47–58

    Article  Google Scholar 

  37. Boer SI, Hedtkamp SIC, van Beusekom JEE, Fuhrman JA, Boetius A, Ramette A (2009) Time- and sediment depth-related variations in bacterial diversity and community structure in subtidal sands. ISME J 3: 780–791. http://www.nature.com/ismej/journal/v3/n7/suppinfo/ismej200929s1.html

  38. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055

    Article  Google Scholar 

  39. Braak CJFtaŠ, P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination version 4.5

  40. Zwart G, Crump BC, Agterveld M, 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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. McArthur JV, Kovacic DA, Smith MH (1988) Genetic diversity in natural populations of a soil bacterium across a landscape gradient. Proc Natl Acad Sci U S A 85:9621–9624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Langenheder S, Ragnarsson H (2007) The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology 88:2154–2161

    Article  PubMed  Google Scholar 

  44. Lindstrom 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. doi:10.1128/aem.71.12.8201-8206.2005

    Article  PubMed  PubMed Central  Google Scholar 

  45. Logue JB, Lindstrom ES (2010) Species sorting affects bacterioplankton community composition as determined by 16S rDNA and 16S rRNA fingerprints. Isme J 4:729–738

    Article  CAS  PubMed  Google Scholar 

  46. Wallace JB, Eggert SL, Meyer JL, Webster JR (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–104. doi:10.1126/science.277.5322.102

    Article  CAS  Google Scholar 

  47. Kritzberg ES, Langenheder S, Lindstrom ES (2006) Influence of dissolved organic matter source on lake bacterioplankton structure and function—implications for seasonal dynamics of community composition. FEMS Microbiol Ecol 56:406–417

    Article  CAS  PubMed  Google Scholar 

  48. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems—a cross-system overview. Marine Ecol Prog Series 43:1–10

    Article  Google Scholar 

  49. Kritzberg ES, Cole JJ, Pace MM, Graneli W (2006) Bacterial growth on allochthonous carbon in humic and nutrient-enriched lakes: results from whole-lake 13C addition experiments. Ecosystems 9:489–499

    Article  CAS  Google Scholar 

  50. Kritzberg ESCJ, Pace ML, Granéli W, Bade D (2004) Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnol Oceanogr 49(2):588–596

    Article  CAS  Google Scholar 

  51. Caron DA (1994) Inorganic nutrients, bacteria, and the microbial loop. Microb Ecol 28:295–298. doi:10.1007/bf00166820

    Article  CAS  PubMed  Google Scholar 

  52. Downing JA, Osenberg CW, Sarnelle O (1999) Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecology 80:1157–1167. doi:10.1890/0012-9658(1999)080[1157:maomne]2.0.co;2

    Article  Google Scholar 

  53. Fisher MM, Klug JL, Lauster G, Newton M, Triplett EW (2000) Effects of resources and trophic interactions on freshwater bacterioplankton diversity. Microb Ecol 40:125–138. doi:10.1007/s002480000049

    CAS  PubMed  Google Scholar 

  54. Steger K, Jarvis Å, Vasara T, Romantschuk M, Sundh I (2007) Effects of differing temperature management on development of Actinobacteria populations during composting. Res Microbiol 158:617–624

    Article  CAS  PubMed  Google Scholar 

  55. Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, Schlesner H, Jenkins C, Staley J (2006) The phylum Verrucomicrobia: a phylogenetically heterogeneous bacterial group. The prokaryotes. Springer New York, pp. 881–896

  56. Ratledge C (1982) Nutrition, growth and metabolism. In: Ratledge C, Stanford J (eds) The biology of the Mycobacteria. Academic Press. London, UK

    Google Scholar 

  57. Hahn MW MA, Lang E, Koll U, Sproer C (2011) Polynucleobacter difficilis sp. nov., a planktonic freshwater bacterium affiliated with subcluster B1 of the genus Polynucleobacter. Int J Syst Evol Microbiol: ijs.0.031393-031390v031391-ijs.031390.031393-031390.

  58. Jezbera J, Jezberova J, Brandt U, Hahn MW (2011) Ubiquity of Polynucleobacter necessarius subspecies asymbioticus results from ecological diversification. Environ Microbiol 13:922–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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 67:57–68

    Article  CAS  PubMed  Google Scholar 

  60. Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927

    Article  Google Scholar 

  61. Schutte UME, Abdo Z, Foster J, Ravel J, Bunge J, Solheim B, Forney LJ (2010) Bacterial diversity in a glacier foreland of the high Arctic. Mol Ecol 19:54–66

    Article  PubMed  Google Scholar 

  62. Webster NS, Taylor MW, Behnam F, Lucker S, Rattei T, Whalan S, Horn M, Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 11:1701–1712

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr Terry Marsh, Dr Dave Long, and Dr Thomas Voice for their critical suggestions and discussions; Matthew Parsons for his help with the ICP-MS analyses and GIS; Shawn McElmurry for the assistance in designing the field sampling protocols; Natasha Isaacs and Fan Yang for the help of T-RFLP and 454 analysis; Ederson Jesus for the PCA analysis; Jurg Logue for the discussion on multivariable analysis; Jenni van Ravensway for also helping with GIS; and Seth Hunt for his help in phosphorous analysis.

Author information

Authors and Affiliations

  1. Environmental Microbiology and Ecology Research Center, Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing, 401122, China

    Liyan Song & Lei Li

  2. Department of Civil and Environmental Engineering, Michigan State University, East Lansing, MI, 48824, USA

    Liyan Song

Authors
  1. Liyan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liyan Song.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 611 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, L., Li, L. Variations in Bacterial Community in a Temperate Lake Associated with an Agricultural Watershed. Microb Ecol 72, 277–286 (2016). https://doi.org/10.1007/s00248-016-0783-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0783-z

Keywords

Search

Navigation