Aquatic Sciences

, Volume 74, Issue 3, pp 513–525 | Cite as

Carbon quantity defines productivity while its quality defines community composition of bacterioplankton in subarctic ponds

  • Toni Roiha
  • Marja Tiirola
  • Matteo Cazzanelli
  • Milla Rautio
Research Article


Bacterial communities in 16 oligotrophic ponds in Kilpisjärvi, subarctic Finland, were studied to test the hypothesis that dissolved organic carbon (DOC) quantity and quality differently influence bacterioplankton. The ponds were located below and above treeline at 600 m a.s.l., with 2–4 fold higher concentration of DOC below treeline. The concentration of DOC changed during the open-water season with highest values measured in mid-summer. Bacterial production, abundance, biomass were highest in mid-summer and correlated positively with the concentration of DOC. Quality indices of DOC showed that spring differed from the rest of the season. Highest specific UV-absorbance (SUVA) and humification index (HI), ratio a250/a265 and lowest fluorescence index (FI) were found during spring compared to summer and autumn, possibly indicating higher relative importance of allochthonous carbon during spring and a seasonal effect of photo-oxidation. According to Length Heterogeneity Polymerase Chain Reaction (LH-PCR) analyses, bacterial communities in spring were significantly different from those later in the season, possible due to the introduction of terrestrial bacteria associated with higher molecular weight material in spring DOC. Comparison between ponds situated above and below treeline revealed that bacteria were more abundant and productive at lower altitudes, which is probably connected to higher concentrations of DOC. The results also suggest that increased temperature and precipitation induced by global change and consequent higher allochthonous DOC runoff from the catchment could have a strong impact on biomass, productivity and community composition of micro-organisms in subarctic ponds and lakes.


Subarctic DOC Ponds Bacterial biomass Bacterial production Bacterial community composition Allochthonous carbon 



We thank Laura Forsström, Heather Mariash and Jonna Kuha for assistance in the field, Timo Marjomäki, Heikki Hämäläinen and Mathieu Cusson for advice on statistical analyses, and Roger Jones for comments on an earlier manuscript version. We thank Kilpisjärvi biological station for hospitability during field work. The study was supported by the Societas pro Fauna et Flora Fennica, the Haavikko Foundation, Lapland Atmosphere-Biosphere Facility and the Finnish Academy of Science (grants 119205 and 140775).


  1. ACIA (2005) Arctic climate impact assessment. Cambridge University Press, New YorkGoogle Scholar
  2. Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12:1319–1333PubMedCrossRefGoogle Scholar
  3. Baron J, McKnight DM, Denning AS (1991) Sources of dissolved and particulate organic material in Loch Vale watershed, Rocky Mountain National Park, Colorado, USA. Biogeochem 15:89–110CrossRefGoogle Scholar
  4. Bjørnsen PK (1986) Automatic determination of bacterioplankton biomass by image analysis. Appl Environ Microbiol 51:1199–1204PubMedGoogle Scholar
  5. Blom T, Korhola A, Weckström J, Laing T, Snyder J, MacDonald G, Smol J (2000) Physical and chemical characterization of small subarctic headwater lakes in Finnish Lapland and Kola Peninsula. Verh Int Ver Limnol 27:316–320Google Scholar
  6. 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
  7. Forsström L, Sorvari S, Rautio M, Sonninen E, Korhola A (2007) Changes in physical and chemical limnology and plankton during the spring melt period in a subarctic lake. Int Rev Hydrobiol 92:301–325CrossRefGoogle Scholar
  8. Fry JC (1988) Determination of biomass. In: Austin B (ed) Methods in aquatic bacteriology. John Wiley & Sons, New York, pp 27–72Google Scholar
  9. Granéli W, Bertilsson S, Philibert A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66:430–439CrossRefGoogle Scholar
  10. Hahn MW, Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35:113–121PubMedCrossRefGoogle Scholar
  11. Hanson PC, Bade DL, Carpenter SR, Kratz TK (2003) Lake metabolism: Relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–1119CrossRefGoogle Scholar
  12. Hessen DO, Andersen T, Lyche A (1990) Carbon metabolism in a humic lake: Pool sizes and cycling through zooplankton. Limnol Oceanogr 35:84–99CrossRefGoogle Scholar
  13. Hessen DO, Blomqvist P, Dahl-Hansen G, Drakare S, Lindström ES (2004) Production and food web interactions of Arctic freshwater plankton and responses to increased DOC. Arch Hydrobiol 159:289–307CrossRefGoogle Scholar
  14. Hobbie JE, Laybourn-Parry J (2008) Heterotrophic microbial processes in polar lakes. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers–limnology of arctic and antarctic aquatic ecosystems. Oxford University Press, Oxford, pp 197–212Google Scholar
  15. Hobbie JE, Daley RJ, Jasper S (1977) Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228PubMedGoogle Scholar
  16. Hobbie JE, Traaen T, Rublee PA, Reed JP, Miller MC, Fenchel T (1980) Decomposers, bacteria, and microbenthos. In: Hobbie JE (ed) Limnology of tundra ponds Barrow. Alaska, Hutchinson & Ross, pp 340–387CrossRefGoogle Scholar
  17. Hobbie JE, Bahr M, Bettez N, Rublee PA (2000) Microbial food webs in oligotrophic arctic lakes. Microbial Biosystems: New Frontiers, Proceedings of the 8th international symposium on Microbial Ecology. Atlantic Canada society for Microbial Ecology, Halifax, Canada, pp 293–298Google Scholar
  18. Hood E, McKnight DM, Williams MW (2003) Sources and chemical quality of dissolved organic carbon (DOC) across an alpine/subalpine ecotone, Green Lakes Valley, Colorado Front Range, United States. Wat Resour Res 39:1188CrossRefGoogle Scholar
  19. Hood E, Williams MW, McKnight DM (2005) Sources of dissolved organic matter (DOM) in a Rocky Mountain stream using chemical fractionation and stable isotopes. Biogeochem 74:231–255CrossRefGoogle Scholar
  20. Jaffe R, McKnight DM, Maie N, Cory R, McDowell WH, Campbell JL (2008) Spatial and temporal variations in DOM composition in ecosystems: The importance of long-term monitoring of optical properties. J Geophys Res 113:G04032CrossRefGoogle Scholar
  21. Jansson M, Blomqvist P, Jonsson A, Bergström A-K (1996) Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnol Oceanogr 41:1552–1559CrossRefGoogle Scholar
  22. Jansson M, Bergström A-K, Blomqvist P, Isaksson A, Jonsson A (1999) Impact of allochthonous organic carbon on microbial food web carbon dynamics and structure in Lake Örträsket. Arch Hydrobiol 144:409–428Google Scholar
  23. Jeffrey SW, Walschmeyer NA (1997) Spetrophotometric and fluorometric equations in common use in oceanography. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography. UNESCO publishing, Paris, pp 361–381Google Scholar
  24. Jones RI (1992) The influence of humic substances on lacustrine planktonic food-chains. Hydrobiol 229:73–91CrossRefGoogle Scholar
  25. Jürgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Ant van Leeuwen 81:413–434CrossRefGoogle Scholar
  26. Kalbitz K, Geyer W, Geyer S (1999) Spectroscopic properties of dissolved humic substances—a reflection of land use history in a fen area. Biogeochem 47:219–238Google Scholar
  27. Kankaala P (1988) The relative importance of algae and bacteria as food for Daphnia longispina (Cladocera) in a polyhumic lake. Freshw Biol 19:285–296CrossRefGoogle Scholar
  28. Karlsson J, Jonsson A, Jansson M (2001) Bacterioplankton production in lakes along an altitude gradient in the subarctic north of Sweden. Microb Ecol 42:372–382PubMedCrossRefGoogle Scholar
  29. Karlsson J, Jansson M, Johnsson A (2002) Similar relationships between pelagic primary and bacterial production in clearwater and humic lakes. Ecol 83:2902–2910CrossRefGoogle Scholar
  30. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of 554 nutrient-poor lake ecosystems. Nature 460:506–510PubMedCrossRefGoogle Scholar
  31. Kirchman D, K’nees E, Hodson RE (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607PubMedGoogle Scholar
  32. Kritzberg ES, Cole JJ, Pace ML, Granéli W, Bade DL (2004) Autochthonous vs. allochthonous carbon sources to bacteria: results from whole-lake 13C experiments. Limnol Oceanogr 49:588–596CrossRefGoogle Scholar
  33. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Chichester, pp 115–175Google Scholar
  34. Laurion I, Vincent WF, Lean DRS (1997) Underwater ultraviolet radiation: development of spectral models for northern latitude lakes. Photochem Photobiol 65:107–114Google Scholar
  35. Laurion I, Vincent WF, MacIntyre S, Retamal L, Dupont C, Francus P, Pienitz (2010) Variability in greenhouse emissions from permafrost thaw ponds. Limnol Oceanogr 55:115-133Google Scholar
  36. Laybourn-Parry J, Marshall WA (2003) Photosynthesis, mixotrophy and microbial plankton dynamics in two high Arctic lakes during summer. Polar Biol 26:517–524CrossRefGoogle Scholar
  37. Lindell MJ, Granéli HW, Tranvik LJ (1995) Enhanced bacterial growth in response to photochemical transformation of dissolved organic matter. Limnol Oceanogr 40:195–199CrossRefGoogle Scholar
  38. Lindell MJ, Granéli HW, Tranvik LJ (1996) Effects of sunlight on bacterial growth in lakes of different humic content. Aquat Microb Ecol 11:135–141CrossRefGoogle Scholar
  39. Mariash HL, Cazzanelli M, Kainz MJ, Rautio M (2011) Zooplankton nutrient sources and lipid retention in subarctic ponds. Freshwat Biol (in press)Google Scholar
  40. McGuire AD, Anderson LG, Christensen TR, Dallimore S, Guo L, Hayes DJ, Heimann M, Lorenson TD, Macdonald RW, Roulet N (2009) Sensitivity of the carbon cycle in the Arctic to climate change. Ecol Monogr 79:523–555CrossRefGoogle Scholar
  41. McKnight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT (2001) Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46:38–48CrossRefGoogle Scholar
  42. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  43. Mitchell BG, Kahru M, Wieland J, Stramska M (2003) Determination of spectral absorption coefficients of particles, dissolved material and phytoplankton for discrete water samples. In: Mueller JL, Fargion GS, McClain CR (eds) Ocean optics protocols for satellite ocean color sensor validation, Revision 4, vol IV, NASA/TM-2003–211621/R. Goddard Space Flight Center, Greenbelt, pp 39–56Google Scholar
  44. Mobed JJ, Hemmingsen SL, Autry JL, McGown LB (1996) Fluorescence characterization of IHSS humic substances: total luminescence spectra with absorbance correction. Environ Sci Technol 30:3061–3065CrossRefGoogle Scholar
  45. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700PubMedGoogle Scholar
  46. Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigment determination. Arch Hydrobiol Beih 14:14–36Google Scholar
  47. O’Brien WJ, Bahr M, Hershey AE, Hobbie JE, Kipphut GW, Kling HK, McDonald M, Miller MC, Rublee P, Vestal JR (1997) The limnology of Toolik Lake. In: Milner AM, Oswood MW (eds) Freshwaters of Alaska. Springer-verlag, New York, pp 61–106CrossRefGoogle Scholar
  48. Ochs CA, Cole JL, Likens GE (1995) Population dynamics of bacterioplankton in an oligotrophic lake. J Plankton Res 17:365–391CrossRefGoogle Scholar
  49. 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
  50. Panzenböck M, Möbes-Hansen B, Albert R, Herndl GJ (2000) Dynamics of phyto- and bacterioplankton in a high Arctic lake on Franz Joseph Land archipelago. Aquat Microb Ecol 21:265–273CrossRefGoogle Scholar
  51. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  52. Prentki RT, Miller MC, Barsdate RJ, Alexander V, Kelley J, Coyne P (1980) Chemistry. In: Hobbie JE (ed) Limnology of tundra ponds Barrow. Alaska, Hutchinson & Ross, Dowden, pp 76–179Google Scholar
  53. Rae R, Vincent WF (1998) Effects of temperature and ultraviolet radiation on microbial food web structure: potential responses to global change. Freshw Biol 40:747–758CrossRefGoogle Scholar
  54. Rautio M (1998) Community structure of crustacean zooplankton in subarctic ponds—effects of altitude and physical heterogeneity. Ecography 21:327–335CrossRefGoogle Scholar
  55. Rautio M (2001) Zooplankton assemblages related to environmental characteristics in treeline ponds in Finnish Lapland. Arct Antarct Alp Res 33:289–298CrossRefGoogle Scholar
  56. Rautio M, Vincent WF (2007) Isotopic analysis of the sources of organic carbon for zooplankton in shallow subarctic and arctic waters. Ecography 30:77–87Google Scholar
  57. Salonen K, Arvola L, Tulonen T, Hammar T, Metsälä T-R, Kankaala P, Münster U (1992) Planktonic food chains of a highly humic lake. Hydrobiol 229:125–142CrossRefGoogle Scholar
  58. Sawström C, Laybourn-Parry J, Granéli W, Anesio AM (2007) Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiment. Polar Biol 30:1407–1415CrossRefGoogle Scholar
  59. Selinummi J, Seppälä J, Yli-Harja O, Puhakka JA (2005) Software for quantification of labeled bacteria from digital microscope images by automated image analysis. Biotechniques 39:859–863PubMedCrossRefGoogle Scholar
  60. Simon M, Azam F (1989) Protein-content and protein-synthesis rates of planktonic marinebacteria. Mar Ecol Prog Ser 51:201–213CrossRefGoogle Scholar
  61. Simon M, Tilzer MM, Müller H (1998) Bacterioplankton dynamics in a large mesotrophic lake: I. Abundance, production and growth control. Arch Hydrobiol 143:385–407Google Scholar
  62. Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114Google Scholar
  63. Stedmon CA, Markager S, Kaas H (2000) Optical properties and signatures of chromophoric dissolved organic matter (CDOM) in Danish coastal waters. Estuar Coast Shelf Sci 51:267–278CrossRefGoogle Scholar
  64. Stewart AJ, Wetzel RG (1980) Fluorescence : absorbance ratios—a molecular-weight tracer of dissolved organic matter. Limnol Oceanogr 25:559–564CrossRefGoogle Scholar
  65. Suzuki MT, Rappé MS, Giovannoni SJ (1998) Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64:4522–4529PubMedGoogle Scholar
  66. Taipale S, Jones RI, Tiirola MA (2009) Vertical diversity of bacteria in an oxygen-stratified humic lake, evaluated using DNA and phospholipid analyses. Aquat Microb Ecol 55:1–16CrossRefGoogle Scholar
  67. Tiirola MA (2002) Phylogenetic analysis of bacterial diversity using ribosomal RNA gene sequences. Dissertation, University of JyväskyläGoogle Scholar
  68. Tranvik LJ (1988) Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb Ecol 16:311–322CrossRefGoogle Scholar
  69. Tranvik LJ (1998) Degradation of dissolved organic matter in humic water by bacteria. In: Hessen DO, Tranvik LJ (eds) Aquatic humic substances—ecology and biochemistry, Springer, Berlin, pp 259–284Google Scholar
  70. Tulonen T (1993) Bacterial production in a mesohumic lake estimated from [C-14] leucine incorporation rate. Microb Ecol 26:201–217CrossRefGoogle Scholar
  71. Vincent WF, Pienitz R (1996) Sensitivity of high latitude freshwater ecosystems to global change: temperature and solar ultraviolet radiation. Geosci Can 23:231–236Google Scholar
  72. Vrede K (2005) Nutrient and temperature limitation of bacterioplankton growth in temperate lakes. Microb Ecol 49:245–256PubMedCrossRefGoogle Scholar
  73. Walter KM, Zimov SA, Chanton JP, Verbyla D, Chapin FS III (2006) Methane bubbling from Siberian thaw lakes as a positive feedback to climate warming. Nature 443:71–75PubMedCrossRefGoogle Scholar
  74. Weishaar JL, Aiken GR, Bergamaschi BA, Fram MS, Fujii R, Mopper K (2003) Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environ Sci Technol 37:4702–4708PubMedCrossRefGoogle Scholar
  75. Wetzel RG, Hatcher PG, Bianchi TS (1995) Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism. Limnol Oceanogr 40:1369–1380CrossRefGoogle Scholar
  76. Wiebe WJ, Sheldon WM Jr, Pomeroy LR (1992) Bacterial growth in the cold: evidence for an enhanced substrate requirement. Appl Environ Microbiol 58:359–364PubMedGoogle Scholar
  77. Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Res 10:221–231Google Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Toni Roiha
    • 1
    • 2
  • Marja Tiirola
    • 1
  • Matteo Cazzanelli
    • 3
  • Milla Rautio
    • 1
    • 2
  1. 1.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland
  2. 2.Département des sciences fondamentalesCentre for Northern Studies (CEN), Université du Québec à ChicoutimiQuébecCanada
  3. 3.Freshwater Biological LaboratoryUniversity of CopenhagenHillerødDenmark

Personalised recommendations