Abstract
Nitrogen and phosphorus additions from anthropogenic sources can alter the nutrient pool of aquatic systems, both through increased nutrient concentrations and changes in stoichiometry. Because bacteria are important in nutrient cycling and aquatic food webs, information about how nutrients affect bacterial communities enhances our understanding of how changes in nutrient concentrations and stoichiometry potentially affect aquatic ecosystems as a whole. In this study, bacterial communities were examined in biofilms from cobbles collected across seasons at three sites along the Mahoning River (Ohio) with differing levels of inorganic nutrient inputs. Members of the alpha-, beta-, and gamma-proteobacteria, the Cytophaga–Flavobacteria cluster, and the Domain Bacteria were enumerated using fluorescent in situ hybridization. Detrended canonical correspondence analysis (DCCA) revealed that stoichiometric ratios, especially the dissolved inorganic nitrogen (DIN):soluble reactive phosphorus (SRP) molar ratio (NO2/NO3 + NH4:soluble reactive phosphorus), were correlated with abundance of the various bacterial taxa. However, the patterns were complicated by correlations with single nutrient concentrations and seasonal changes in temperature. Seasonal cycles appeared to play an important role in structuring the community, as there were distinct winter communities and temperature was negatively correlated with abundance of both alpha-proteobacteria and Cytophaga–Flavobacteria. However, nutrients and stoichiometry also appeared to affect the community. Numbers of cells hybridizing the Domain Bacteria probe were correlated with the DOC:DIN ratio, the beta-proteobacteria had a negative correlation with soluble reactive phosphorus concentrations and a positive correlation with the DIN:SRP ratio, and the Cytophaga–Flavobacteria had a significant negative partial correlation with the DIN:SRP ratio. Abundances of the alpha- or gamma-proteobacteria were not directly correlated to nutrient concentrations or stoichiometry. It appears that nutrient stoichiometry may be an important factor structuring bacterial communities; however, it is one of many factors, such as temperature, that are interlinked and must be considered together when studying environmental bacteria.
Similar content being viewed by others
References
Amann, RI, Binder, BJ, Olson, RJ, Chisholm, SW, Devereux, R, Stahl, DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry and analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919–1925
Amann, RI (1995) In situ identification of microorganisms by whole cell hybridization with rRNA-targeted nucleic acid probes. Mol Microbiol Ecol Manual 3.3.6: 1–15
Araya, R, Tani, K, Takagi, T, Yamaguchi, N, Nasu, M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent In situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43: 111–119
Battin, TJ, Wille, A, Sattler, B, Psenner, R (2001) Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microbiol 67: 799–807
Brett, MT, Lubnow, FS, Villar-Argaiz, M, Müller-Solger, A, Goldman, CR (1999) Nutrient control of bacterioplankton and phytoplankton dynamics. Aquat Ecol 33: 135–145
Brümmer, IHM, Felske, A, Wagner-Döbler (2003) Diversity and seasonal variability of β-proteobacteria in biofilms of polluted rivers: analysis by temperature gradient gel electrophoresis and cloning. Appl Environ Microbiol 69: 4463–4473
Chrzanowski, TH, Kyle, M (1996) Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration. Aquat Microb Ecol 10: 115–122
Cross, WF, Benstead, JP, Frost, PC, Thomas, SA (2005) Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Freshw Biol 50: 1895–1912
Elser, JJ, Fagan, WF, Denno, RF, Dobberfuhl, DR, Folarin, A, Huberty, A, Interlandi, S, Kilham, SS, McCauley, E, Schulz, KL, Siemann, EH, Sterner, RW (2000) Nutritional constraints in terrestrial and freshwater foodwebs. Nature 408: 578–580
Elser, JJ, Urabe, J (1999) The stoichiometry of consumer-driven nutrient cycling: theory, observations, and consequences. Ecology 80: 735–751
Fisher, MM, Klug, JL, Lauster, G, Newton, M, Triple, EW (2000) Effects of resources and trophic interactions on freshwater bacterioplankton diversity. Microb Ecol 40: 125–138
Frost, PC, Stelzer, RS, Lamberti, GA, Elser, JJ (2002) Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C:N:P ratios in lentic and lotic habitats. J North Am Benthol Soc 21: 515–528
Gao, X, Olapade, OA, Leff, LG (2005) Comparison of benthic bacterial community composition in nine streams. Aquat Microb Ecol 40: 51–60
Geller, A (1986) Comparison of mechanisms enhancing biodegradability of refractory lake water constituents. Limnol Oceanogr 31: 755–764
Granéli, W, Bertilsson, S, Philibert, A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66: 430–439
Hessen, DO (1992) Nutrient element limitation of zooplankton production. Am Nat 140: 799–814
Jardillier, L, Boucher, D, Personnic, S, Jacquet, S, Thénot, A, Sargos, D, Amblard, C, Debroas, D (2005) Relative importance of nutrients and mortality factors on prokaryotic community composition in two lakes of different trophic status: microcosm experiments. FEMS Microbiol Ecol 53: 429–443
Jezbera, J, Horňák, K, Šimek, K (2005) Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence In situ hybridization. FEMS Microbiol Ecol 52: 351–363
Keinänen, MM, Korhonen, LK, Lehtola, MJ, Miettinen, IT, Martikainen, PJ, Vartianinen, T, Suutari, MH (2002) The microbial community structure of drinking water biofilms can be affected by phosphorus availability. Appl Environ Microbiol 68: 434–439
Kent, AD, Jones, SE, Yannarell, AC, Graham, JM, Lauster, GH, Kratz, TK, Triplett EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol 48: 550–560
Kirchman, DL (2002) The ecology of Cytophaga–flavobacteria in aquatic environments. FEMS Microbiol Ecol 39: 91–100
Kroer, N (1993) Bacterial growth efficiency on natural dissolved organic matter. Limnol Oceanogr 38: 1282–1290
Leff, LG, Brown, BJ, Lemke, MJ (1999) Spatial and temporal changes in bacterial assemblages of the Cuyahoga River. Ohio J Sci 99: 44–48
Lemke, MJ, McNamara, CJ, Leff, LG (1997) Comparison of methods for the concentration of bacterioplankton for In situ hybridization. J Microbiol Methods 29: 23–29
Makino, W, Cotner, JB, Sterner, RW, Elser, JJ (2003) Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C:N:P stoichiometry. Funct Ecol 17: 121–130
Manz, W, Wendt-Potthoff, K, Neu, TR, Szewzyk, U, Lawrence, JR (1999) Phylogenetic composition, spatial structure, and dynamics of lotic bacterial biofilms investigated by fluorescent In situ hybridization and confocal scanning laser microscopy. Microb Ecol 37: 225–237
Martinez, J, Smith, DC, Steward, GF, Azam, F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10: 223–230
McNamara, CJ, Leff, LG (2004) Bacterial community composition in biofilms on leaves in a northeastern Ohio stream. J North Am Benthol Soc 23: 677–685
Methé, BA, Zehr, JP (1999) Diversity of bacterial communities in Adirondack lakes: do species assemblages reflect lake water chemistry? Hydrobiologia 401: 77–96
Meyer, JL (1994) The microbial loop in flowing waters. Microb Ecol 28: 195–199
Mohamed, MN, Robarts, RD (2003) Sestonic bacterial nutrient limitation in a northern temperate river and the impact of pulp-mill effluents. Aquat Microb Ecol 33: 19–28
Nakano, SI (1994) Carbon:nitrogen:phosphorus ratios and nutrient regeneration of a heterotrophic flagellate fed on bacteria with different elemental ratios. Arch Hydrobiol 129: 257–271
Olapade, OA, Leff, LG (2003) The effect of toluene on the microbial community of a river in Northeastern Ohio, USA. J Freshw Ecol 18: 465–477
Olapade, OA, Leff, LG (2004) Seasonal dynamics of bacterial assemblages in epilithic biofilms in a northeastern Ohio stream. J North Am Benthol Soc 23: 686–700
Olapade, OA, Leff, LG (2005) Seasonal response of stream biofilm communities to dissolved organic matter and nutrient enrichments. Appl Environ Microbiol 71: 2278–2287
Pinhassi, J, Berman, T (2003) Differential growth response of colony forming α and γ-proteobacteria in dilution culture and nutrient addition experiments from lake Kinneret (Israel), the eastern Mediterranean Sea, and the Gulf of Eilat. Appl Environ Microbiol 69: 199–211
Porter, KG, Feig, YS (1980) The use of DAPI for indentifying and counting aquatic microflora. Limnol Oceanogr 25: 943–948
Purkhold, U, Wagner, M, Timmermann, G, Pommerening-Roeser, A, Koops, H-P (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53: 1485–1494
Rejas, D, Muylaert, K, De Meester, L (2005) Nutrient limitation of bacteria and sources of nutrients supporting nutrient-limited bacterial growth in an Amazonian floodplain lake. Aquat Microbial Ecol 39: 57–67
Schweitzer, B, Huber, I, Amann, R, Ludwig, W, Simon, M (2001) α- and β-proteobacteria control the consumption and release of amino acids on lake snow aggregates. Appl Environ Microbiol 67: 632–645
Shi, Y, Zwolinski, MD, Schreiber, ME, Bahr, JM, Sewell, GW, Hickey, WJ (1999) Molecular analysis of microbial community structures in pristine and contaminated aquifers: field and laboratory microcosm experiments. Appl Environ Microbiol 65: 2143–2150
State of Ohio Environmental Protection Agency (1996) Biological and water quality study of the Mahoning River basin. OEPA Technical Report MAS/1995-12-14 Vol 1
Tank, JL, Webster, JR (1998) Interaction of substrate and nutrient availability on wood biofilm processes in streams. Ecology 79: 2168–2179
Tezuka, JE (1990) Bacterial regeneration of ammonium and phosphate as affected by the carbon–nitrogen–phosphorus ratio of organic substrates. Microb Ecol 19: 227–238
Tilman, D, Kilham, SS, Kilham, P (1982) Phytoplankton community ecology: the role of limiting nutrients. Annu Rev Ecol Syst 13: 349–372
Turner, RE, Rabalais, NN, Dortch, Q (2003) Global patterns of dissolved N, P and Si in large rivers. Biogeochemistry 64: 297–317
Vadstein, O (2000) Heterotrophic, planktonic bacteria and cycling of phosphorus: phosphorus requirements, competitive ability, and food web interactions. In: Schink, B (Ed.) Advances in Microbial Ecology, vol. 16, Kluwer Academic/Plenum Publishers, New York, pp 115–167
Vitousek, PM, Aber, JD, Howarth, RW, Likens, GE, Matson, PA, Schindler, DW, Schlesinger WH, Tilman DG (1997) Technical report: human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7: 737–750
Xu, P, Leff, LG (2004) Longitudinal changes in the benthic bacterial community of the Mahoning River (Ohio, USA). Hydrobiologia 522: 329–335
Yokokawa, T, Nagata, T (2005) Growth and grazing mortality rates of phylogenetic groups of bacterioplankton in coastal marine environments. Appl Environ Microbiol 71: 6799–6807
Zwisler, W, Natascha, S, Meinhard, S (2003) Seasonal patterns of the bacterioplankton community composition in a large mesotrophic lake. Aquat Microb Ecol 31: 211–222
Acknowledgements
Thanks to Kent State University for support of this research and Todd Royer for his assistance and advice.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rubin, M.A., Leff, L.G. Nutrients and Other Abiotic Factors Affecting Bacterial Communities in an Ohio River (USA). Microb Ecol 54, 374–383 (2007). https://doi.org/10.1007/s00248-007-9209-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-007-9209-2