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Periphytic Photosynthetic Stimulation of Extracellular Enzyme Activity in Aquatic Microbial Communities Associated with Decaying Typha Litter

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Abstract

We examined the effect of light on extracellular enzyme activities of periphytic/endogenous microbial assemblages associated with decomposing litter of an emergent macrophyte Typha angustifolia within a small inland wetland in southeastern Michigan. Standing-dead Typha leaf litter was collected, placed into floating wire mesh litter baskets, and submerged in a wetland pool. Enzyme saturation assays were conducted on three occasions following litter submergence (days 9, 28, and 44) to generate saturation curves for the individual enzymes tested and to examine potential differences in enzyme saturation kinetics during microbial colonization and development. Experimental light manipulations were conducted on two occasions during microbial development (days 10 and 29). Short-term (30 min) light exposure significantly increased extracellular β-glucosidase activity of litter-associated microbial communities. Activities of β-xylosidase and leucine-aminopeptidase were not stimulated, and stimulation of phosphatase activity was variable. The exact mechanism for increased enzyme activity remains unknown, but it may have been increased pH arising from periphytic algal photosynthesis. These results suggest that extracellular enzyme activity in microbial communities colonizing natural organic substrata may be influenced by light/photosynthesis, as has previously been demonstrated for periphyton communities grown on artificial, inert substrata. Thus, light/photosynthetic mediated stimulation of extracellular enzyme activities may be a common occurrence in microbial communities associated with natural decaying plant litter in wetlands and might engender diurnal patterns in other microbial decay processes (e.g., production, organic matter decomposition, and mineralization).

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References

  1. APHA (1992) Standard Methods for the Examination of Water and Wastewater, 18th edn. American Public Health Association, Washington, DC

    Google Scholar 

  2. Bärlocher, F (1985) The role of fungi in the nutrition of stream invertebrates. Bot J Linn Soc 91: 83–94

    Google Scholar 

  3. Biggs, BJF (1990) Use of relative specific growth rates of periphytic diatoms to assess enrichment of a stream. NZ J Mar Freshw Res 24: 9–18

    Article  CAS  Google Scholar 

  4. Biggs, BJF (1987) Effects of sample storage and mechanical blending on the quantitative analysis of river periphyton. Freshw Biol 18: 120–197

    Article  Google Scholar 

  5. Biggs, BJF, Kilroy, C (2000) Stream Periphyton Monitoring Manual. New Zealand Ministry for the Environment/NIWA, Christchurch, New Zealand

  6. Burkholder, JM, Wetzel, RG (1989) Microbial colonization on natural and artificial macrophytes in a phosphorus-limited, hardwater lake. J Phycol 25: 55–65

    Article  Google Scholar 

  7. Carlton, RG, Wetzel, RG (1988) Phosphorus flux from lake sediments: effect of epipelic algal oxygen production. Limnol Oceanogr 33: 562–570

    CAS  Google Scholar 

  8. Chróst, RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: Chróst, RJ (Ed.) Microbial Enzymes in Aquatic Environments, Springer-Verlag, New York, pp 29–59

    Google Scholar 

  9. Chróst, RJ, Overbeck, J (1987) Kinetics of alkaline phosphatase activity and phosphorus availability in for phytoplankton and bacterioplankton in lake Pluβsee (north German eutrophic lake). Microb Ecol 42: 328–337

    Google Scholar 

  10. Chróst, RJ, Rai, H (1993) Ectoenzyme activity and bacterial secondary production in nutrient-impoverished and nutrient-enriched freshwater mesocosms. Microb Ecol 25: 131–150

    Article  Google Scholar 

  11. Cummins, KW (1974) Structure and function of stream ecosystems. BioScience 24: 631–641

    Article  Google Scholar 

  12. Dodds, WK (1991) Micro-environmental characteristics of filamentous algal communities in flowing freshwaters. Freshw Biol 25: 199–209

    Article  Google Scholar 

  13. Espeland, EM, Wetzel, RG (2001) Effects of photosynthesis on bacterial phosphatase production in biofilms. Microb Ecol 42: 328–337

    Article  CAS  PubMed  Google Scholar 

  14. Espeland, EM, Wetzel, RG (2001) Complexation, stabilization, and UV photolysis of extracellular and surface-bound glucosidase and alkaline phosphatase: implications for biofilm microbiota. Microb Ecol 42: 572–585

    Article  CAS  PubMed  Google Scholar 

  15. Espeland, EM, Francoeur, SN, Wetzel, RG (2001) Influence of algal photosynthesis on biofilm bacterial production and associated glucosidase and xylosidase activities. Microb Ecol 42: 524–530

    Article  CAS  PubMed  Google Scholar 

  16. Findlay, SEG, Dye, S, Kuehn, KA (2002) Microbial growth and nitrogen retention in litter of Phragmites australis compared to Typha angustifolia. Wetlands 22: 616–662

    Article  Google Scholar 

  17. Francoeur, SN, Wetzel, RG (2003) Regulation of periphytic leucine-aminopeptidase activity. Aquat Microb Ecol 31: 249–258

    Google Scholar 

  18. Francoeur, SN, Wetzel, RG, Neely, RK (2001) A new spatially-explicit method for detecting extracellular protease activity in biofilms. Appl Environ Microbiol 67: 4329–4334

    Article  CAS  PubMed  Google Scholar 

  19. Gessner, MO, Newell, SY (2002) Biomass, growth rate, and production of filamentous fungi in plant litter. In: Hurst, CJ, Crawford, RL, Knudsen, GR, McInerney, MJ, Stetzenbach, LD (Eds.) Manual of Environmental Microbiology, 2nd edition, ASM Press, Washington, DC, USA, pp 390–408

    Google Scholar 

  20. Graça, MAS, Maltby, L, Calow, P (1993) Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus. I. Feeding strategies. Oecologia 93: 139–144

    Google Scholar 

  21. Gulis, V, Suberkropp, K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48: 123–134

    Article  Google Scholar 

  22. Hall, RO, Jr, Meyer, JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79: 1995–2012

    Article  Google Scholar 

  23. Hameed, HA, Kilinc, S, McGowan, S, Moss, B (1999) Physiological tests and bioassays: Aids or superfluities to the diagnosis of phytoplankton nutrient limitation? A comparative study in the Broads and the Meres of England. Eur J Phycol 34: 253–269

    Article  Google Scholar 

  24. Hoppe, HG (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11: 299–308

    CAS  Google Scholar 

  25. Hoppe, HG, Giesenhagen, HC, Gocke, K (1998) Changing patterns of bacterial substrate decomposition in a eutrophication gradient. Aquat Microb Ecol 15: 1–13

    Google Scholar 

  26. Jones, JI, Eaton, JW, Hardwick, K (2000) The influence of periphyton on boundary layer conditions: a pH microelectrode investigation. Aquat Bot 67: 191–206

    Article  Google Scholar 

  27. Klotz, RL (1985) Factors controlling phosphorus limitation in stream sediments. Limnol Oceanogr 30: 543–553

    CAS  Google Scholar 

  28. Kuehn, KA, Lemke, MJ, Wetzel, RG, Suberkropp, K (2000) Microbial biomass and production associated with decaying leaf litter of the emergent macrophyte Juncus effusus. Limnol Oceanogr 45: 862–870

    Article  CAS  Google Scholar 

  29. Kuehn, KA, Suberkropp, K (1998) Decomposition of standing dead litter of the emergent macrophyte Juncus effusus. Freshw Biol 40: 717–727

    Article  Google Scholar 

  30. Law, BA (1980) Transport and utilization of proteins by bacteria. In: Payne, JW (Ed.) Microorganisms and Nitrogen Sources. John Wiley and Sons, New York, pp 381–409

    Google Scholar 

  31. Li, WKW (1983) Consideration of errors in estimating kinetic parameters based on Michaelis‐Menten formalism in microbial ecology. Limnol Oceanogr 28: 185–190

    CAS  Google Scholar 

  32. Lind, OT (1985) Handbook of Common Methods in Limnology, 2nd edn. Kendall/Hunt, Dubuque, IA

    Google Scholar 

  33. Martinez, J, Azam, F (1993) Aminopeptidase activity in marine chroococcoid cyanobacteria. Appl Environ Microbiol 59: 3701–3707

    CAS  PubMed  Google Scholar 

  34. Matsuda, Y, Koseki, M, Shimadda, T, Saito, T (1995) Purification and characterization of a vegetative lytic enzyme responsible for liberation of daughter cells during the proliferation of Chlamydomonas reinhardtii. Plant Cell Physiol 36: 681–689

    CAS  PubMed  Google Scholar 

  35. Mulholland, PJ (1996) Role in nutrient cycling in streams. In: Stevenson, Bothwell, Lowe (Eds.) Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, pp 609–640

    Google Scholar 

  36. Münster, U (1991) Extracellular enzyme activity in eutrophic and polyhumic lakes. In: Chróst, RJ (Ed.) Microbial Enzymes in Aquatic Environments. Springer-Verlag, New York, NY, pp 96–122

    Google Scholar 

  37. Münster, U (1992) Microbial extracellular enzyme activities and biopolymer processing in two acid polyhumic lakes. Arch Hydrobiol Ergebn Limnol 37: 21–32

    Google Scholar 

  38. Münster, U (1994) Studies on phosphatase activities in humic lakes. Environ Int 20: 49–59

    Article  Google Scholar 

  39. Noble, RT, Fuhrman, JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113–118

    Google Scholar 

  40. Payne, JW (1980) Transport and utilization of peptides by bacteria. In: Payne, JW (Ed.) Microorganisms and Nitrogen Sources. John Wiley and Sons, New York, pp 211–256

    Google Scholar 

  41. Revsbech, NP, Jorgensen, BB, Blackburn, TH, Cohen, Y (1983) Microelectrode studies of the photosynthesis and O2, H2S, and pH profiles of a microbial mat. Limnol Oceanogr 28: 1062–1074

    Article  Google Scholar 

  42. Rego, JV, Billen, G, Fontigny, A, Somvile, M (1985) Free and attached proteolytic activity in water environments. Mar Ecol Prog Ser 21: 245–249

    CAS  Google Scholar 

  43. Richardot, M, Debroas, D, Thouvenot, A, Romagoux, JC, Berthon, JL, Devaux, J (1999) Proteolytic and glycolytic activities in size-fractionated surface water samples from an oligotrophic reservoir in relation to plankton samples. Aquat Sci 61: 279–292

    Article  CAS  Google Scholar 

  44. Rose, C, Axler, RP (1998) Uses of alkaline phosphatase activity in evaluating phytoplankton community phosphorus deficiency. Hydrobiologia 361: 145–156

    Article  Google Scholar 

  45. Sala, MM, Karner, M, Marrasé, C (2001) Measurement of ectoenzyme activities as an indication of inorganic nutrient imbalance in microbial communities. Aquat Microb Ecol 23: 301–311

    Google Scholar 

  46. Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213

    CAS  Google Scholar 

  47. Stevenson, RJ (1996) An introduction to algal ecology in freshwater benthic habitats. In: Stevenson, Bothwell, Lowe (Eds.) Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, pp 3–30

    Google Scholar 

  48. Strepanauskas, R, Edling, H, Tranvik, L (1999) Differential dissolved organic nitrogen availability and bacterial aminopeptidase activity in limnic and marine waters. Microb Ecol 38: 264–272

    Article  Google Scholar 

  49. Sinsabaugh, RL, Carreiro, MM, Alvarez, S (2002) Enzyme and microbial dynamic of litter decomposition. In: Burns, Dick (Ed.) Enzymes in the Environment: Activity, Ecology and Applications. Marcel Dekker Inc, New York, pp 249–265

    Google Scholar 

  50. Sinsabaugh, RL, Findlay, S (1995) Microbial production, enzyme activity, and carbon turnover in surface sediments of the Hudson River estuary. Microb Ecol 30: 127–141

    Article  CAS  Google Scholar 

  51. Sinsabaugh, RL, Linkins, AE (1993) Statistical modeling of litter decomposition from integrated cellulase activity. Ecology 74: 1594–1597

    Article  CAS  Google Scholar 

  52. Sinsabaugh, RL, Osgood, M, Findlay, S (1994) Enzymatic models for estimating decomposition rates of particulate detritus. J North Am Benthol Soc 13: 160–169

    Article  Google Scholar 

  53. Siver, PA (1977) Comparison of attached diatom communities on natural and artificial substrates. J Phycol 13: 402–406

    Article  Google Scholar 

  54. Tuchman, ML, Stevenson, RJ (1980) Comparison of clay tile, sterilized rock, and natural substrate diatom communities in a small stream in southeastern Michigan, USA. Hydrobiologia 75: 73–79

    Article  Google Scholar 

  55. Unanue, M, Azúa, I, Barcina, I, Egea, L, Iriberri, J (1993) Size distribution of aminopeptidase activity and bacterial incorporation of dissolved substrates in three aquatic systems. FEMS Microbiol Ecol 102: 175–183

    Article  CAS  Google Scholar 

  56. Vrba, J, Callieri, C, Bittl, T, Simek, K, Bertoni, R, Filandr, P, Hartman, P, Hejzlar, J, Macek, M, Nedoma, J (2004) Are bacteria the major producers of extracellular glycolytic enzymes in aquatic environments? Int Rev Hydrobiol 89: 102–117

    Article  CAS  Google Scholar 

  57. Wetzel, RG (1996) Benthic algae and nutrient cycling in lentic freshwater ecosystems. In: Stevenson, Bothwell, Lowe (Eds.) Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, pp 641–669

    Google Scholar 

  58. Wetzel, RG (2001) Limnology: Lake and River Ecosystems, 3rd edn. Academic Press, San Diego

    Google Scholar 

  59. Wetzel, RG, Likens, GE (2000) Limnological Analyses, 3rd edn. Springer-Verlag Inc, New York

    Google Scholar 

  60. Weyers, HS, Suberkropp, K (1996) Fungal and bacterial production during the breakdown of yellow poplar leaves in 2 streams. J North Am Benthol Soc 15: 408–420

    Article  Google Scholar 

  61. Wong, MKM, Goh, TH, Hodgkiss, IJ, Hyde, KD, Ranghoo, VM, Tsui, CKM, Ho, WH, Wong, WSW, Yuen, TK (1998) Role of fungi in freshwater ecosystems. Biodivers Conserv 7: 1187–1206

    Article  Google Scholar 

  62. Woodruff, SL, House, WA, Callow, ME, Leadbeater, BSC (1999) The effects of biofilms on chemical processes in surficial sediments. Freshw Biol 41: 73–89

    Article  Google Scholar 

  63. Zar (1999) Biostatistical Analysis, 4th edn. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

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Acknowledgments

The Washtenaw Country Drain Commission provided access to this field site. Audrey Johnson, Valerie Thomas, Brian Ohsowski, Bem Allen, and Serena Byrd provided field and laboratory assistance. Funding for this project was provided by NSF grants DEB0315686 and DEB0423274 and Eastern Michigan University.

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Authors and Affiliations

  1. Department of Biology, Eastern Michigan University, 316 Mark Jefferson Hall, Ypsilanti, MI, 48197, USA

    Steven N. Francoeur, Mark Schaecher & Robert K. Neely

  2. Department of Biological Sciences, The University of Southern Mississippi, 118 College Drive #5018, Hattiesburg, MS 39406, USA

    Kevin A. Kuehn

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  1. Steven N. Francoeur
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  2. Mark Schaecher
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  4. Kevin A. Kuehn
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Correspondence to Steven N. Francoeur.

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Francoeur, S.N., Schaecher, M., Neely, R.K. et al. Periphytic Photosynthetic Stimulation of Extracellular Enzyme Activity in Aquatic Microbial Communities Associated with Decaying Typha Litter. Microb Ecol 52, 662–669 (2006). https://doi.org/10.1007/s00248-006-9084-2

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