Skip to main content
SpringerLink
Log in

Ecoenzymatic Stoichiometry in Relation to Productivity for Freshwater Biofilm and Plankton Communities

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

Abstract

The degradation of detrital organic matter and assimilation of carbon (C), nitrogen (N), and phosphorus (P) by heterotrophic microbial communities is mediated by enzymes released into the environment (ecoenzymes). For the attached microbial communities of soils and freshwater sediments, the activities of β-glucosidase, β-N-acetylglucosaminidase, leucine aminopeptidase, and phosphatase show consistent stoichiometric patterns. To determine whether similar constraints apply to planktonic communities, we assembled data from nine studies that include measurements of these enzyme activities along with microbial productivity. By normalizing enzyme activity to productivity, we directly compared the ecoenzymatic stoichiometry of aquatic biofilm and bacterioplankton communities. The relationships between β-glucosidase and α-glucosidase and β-glucosidase and β-N-acetylglucosaminidase were statistically indistinguishable for the two community types, while the relationships between β-glucosidase and phosphatase and β-glucosidase and leucine aminopeptidase significantly differed. For β-glucosidase vs. phosphatase, the differences in slope (biofilm 0.65, plankton 1.05) corresponded with differences in the mean elemental C:P ratio of microbial biomass (60 and 106, respectively). For β-glucosidase vs. leucine aminopeptidase, differences in slope (0.80 and 1.02) did not correspond to differences in the mean elemental C:N of biomass (8.6 and 6.6). β-N-Acetylglucosaminidase activity in biofilms was significantly greater than that of plankton, suggesting that aminosaccharides were a relatively more important N source for biofilms, perhaps because fungi are more abundant. The slopes of β-glucosidase vs. (β-N-acetylglucosaminidase + leucine aminopeptidase) regressions (biofilm 1.07, plankton 0.94) corresponded more closely to the estimated difference in mean biomass C:N. Despite major differences in physical structure and trophic organization, biofilm and plankton communities have similar ecoenzymatic stoichiometry in relation to productivity and biomass composition. These relationships can be integrated into the stoichiometric and metabolic theories of ecology and used to analyze community metabolism in relation to resource constraints.

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

Figure 1

Similar content being viewed by others

References

  1. Allison SD, Gartner T, Holland K, Weintraub M, Sinsabaugh RL (2007) Soil enzymes: linking proteomics and ecological process. Manual of environmental microbiology. ASM Press, Washington DC, pp 704–711

    Google Scholar 

  2. Allen AP, Gillooly JF (2009) Towards and integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384

    Article  PubMed  Google Scholar 

  3. Artigas J, Romani AM, Sabater S (2008) Relating nutrient molar ratios of microbial attached communities to organic matter utilization in a forested stream. Fund Appl Limnol 173:255–264

    Article  CAS  Google Scholar 

  4. Battin TJ, Kaplan LA, Newbold JD, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442

    Article  CAS  PubMed  Google Scholar 

  5. Biddanda B, Ogdahl M, Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–739

    Article  Google Scholar 

  6. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  7. Burns RG, Dick RP (2002) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York

    Book  Google Scholar 

  8. Cherif M, Loreau M (2007) Stoichiometric constraints on resource use, competitive interactions, and elemental cycling in microbial decomposers. Am Nat 169:709–724

    Article  PubMed  Google Scholar 

  9. Chróst RJ, Siuda W (2003) Ecology of microbial enzymes in lake ecosystems. In: Burns RG, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 35–72

    Google Scholar 

  10. Chrzanowski TH, Kyle M, Elser JJ, Sterner RW (1996) Element ratios and growth dynamics of bacteria in an oligotrophic Canadian shield lake. Aquat Microb Ecol 11:119–125

    Article  Google Scholar 

  11. Cleveland CC, Liptzin D (2006) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  12. Danger M, Daufresne T, Lucas F, Pissard S, Lacroix G (2008) Does Liebig's law of the minimum scale up from species to communities? Oikos 117:1741–1751

    Article  Google Scholar 

  13. Daufresne T, Lacroix G, Benhaim D, Loreau M (2008) Coexistence of algae and bacteria: a test of the carbon hypothesis. Aquat Microb Ecol 53:323–332

    Article  Google Scholar 

  14. Davey ME, O'Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867

    Article  CAS  PubMed  Google Scholar 

  15. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie SE, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943

    Article  Google Scholar 

  16. Findlay S, Sinsabaugh RL (2003) Response of hyporheic biofilm bacterial metabolism and community structure to nitrogen amendments. Aquat Microb Ecol 33:127–136

    Article  Google Scholar 

  17. Findlay S, Sinsabaugh RL (2006) Stream microbial communities: a cross-regional comparison of metabolic function and community similarity. Microb Ecol 52:491–500

    Article  CAS  PubMed  Google Scholar 

  18. Findlay S, Sinsabaugh RL, Fischer DT, Franchini P (1998) Sources of dissolved organic carbon supporting planktonic bacterial production in the tidal freshwater Hudson River. Ecosystems 1:227–239

    Article  CAS  Google Scholar 

  19. Findlay S, Sinsabaugh RL, Sobczak W, Hoostal M (2003) Metabolic and structural response of hyporheic bacterial communities to variations in supply of dissolved organic matter. Limnol Oceanogr 48:1608–1617

    Article  CAS  Google Scholar 

  20. Fischer H, Kloep F, Wilzcek S, Pusch MT (2005) A river’s liver—microbial processes within the hyporheic zone of a large lowland river. Biogeochemistry 76:349–371

    Article  CAS  Google Scholar 

  21. Foreman CM, Franchini P, Sinsabaugh RL (1998) The trophic dynamics of riverine bacterioplankton: relationships among substrate availability, ectoenzyme kinetics and growth. Limnol Oceanogr 43:1344–1352

    Article  CAS  Google Scholar 

  22. Freeman C, Lock M (1995) The biofilm polysaccharide matrix: a buffer against changing organic substrate supply? Limnol Oceanogr 40:273–278

    Article  CAS  Google Scholar 

  23. Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, Yoshida T (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779

    Article  PubMed  Google Scholar 

  24. Geisseler D, Doane TA, Horwath WR (2009) Determining potential glutamine synthetase and glutamate dehydrogenase activity in soil. Soil Biol Biochem 41:1741–1749

    Article  CAS  Google Scholar 

  25. Gusewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  26. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  27. Herron PM, Stark JM, Holt C, Hooker T, Cardon ZG (2009) Microbial growth efficiencies across a soil moisture gradient assessed using 13C-acetic acid vapor and 15N-ammonia gas. Soil Biol Biochem 41:1262–1269

    Article  CAS  Google Scholar 

  28. Hill BH, Elonen CM, Jicha TM, Bolgrien DW, Moffett MF (2009) Sediment microbial enzyme activity as an indicator of nutrient limitation in the great rivers of the Upper Mississippi River basin. Biogeochemistry. doi:10.1007/s10533-009-9366-02009

    Google Scholar 

  29. Hochstadter S (2000) Seasonal changes of C:P ratios of seston, bacteria, phytoplankton and zooplankton in a deep, mesotrophic lake. Freshw Biol 44:453–463

    Article  Google Scholar 

  30. Hoppe H-G, Arnosti C, Herndl GF (2003) Ecological significance of bacterial enzymes in the marine environment. In: Dick RP, Burns RG (eds) Enzymes in the environment. Marcel Dekker, New York, pp 73–108

    Google Scholar 

  31. Interlandi SJ, Killham SS (2001) Limiting resources and the regulation of diversity in phytoplankton communities. Ecology 82:1270–1281

    Article  Google Scholar 

  32. Jansson M, Bergström AK, Lymer D, Vrede K, Karlsson J (2006) Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364

    Article  CAS  PubMed  Google Scholar 

  33. Joint I, Henriksen P, Fonnes GA, Bourne D, Thingstad TF, Riemann B (2002) Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat Microb Ecol 29:145–159

    Article  Google Scholar 

  34. Jorgensen NOG, Kroer N, Coffin RB, Hoch MP (1999) Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem. Aquat Microb Ecol 18:247–261

    Article  Google Scholar 

  35. Karrasch B, Ullrich S, Mehrens M, Zimmerman-Timm H (2004) Free and particle-associated extracellular enzyme activity and bacterial production in the lower Elbe estuary, Germany. Acta Hydrochim Hydrobiol 31:297–306

    Article  Google Scholar 

  36. Kroer N, Jorgensen NOG, Coffin RB (1994) Utilization of dissolved nitrogen by heterotrophic bacterioplankton—a comparison of 3 ecosystems. Appl Environ Microbiol 60:4116–4123

    CAS  PubMed  Google Scholar 

  37. Lebaron P, Servais P, Troussellier M, Courties C, Muyzer G, Bernard L, Schäfer H, Pukall R, Stackebrandt E, Guindulain T, Vives-Rego J (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in abundances, activity and composition. FEMS Microbiol Ecol 34:255–266

    Article  CAS  PubMed  Google Scholar 

  38. 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 

  39. Li B-L, Gorshkov VG, Makarieva AM (2004) Energy partitioning between different-sized organisms and ecosystem stability. Ecology 85:1811–1813

    Article  Google Scholar 

  40. Middelboe M, Sondergaard M (1993) Bacterioplankton growth-yeld—seasonal-variations and coupling to substrate lability and beta-glucosidase activity. Appl Environ Microbiol 59:3916–3921

    CAS  PubMed  Google Scholar 

  41. Redfield A (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221

    CAS  Google Scholar 

  42. Reinthaler T, Herndl GJ (2005) Seasonal dynamics of bacterial growth efficiencies in relation to phytoplankton in the southern North Sea. Aquat Microb Ecol 39:7–16

    Article  Google Scholar 

  43. Romaní AM, Fund K, Artigas J, Schwartz T, Sabater S, Obst U (2008) Relevance of polymeric matrix enzymes during biofilm formation. Microb Ecol 56:427–436

    Article  PubMed  Google Scholar 

  44. Romaní AM, Giorgi A, Acuña V, Sabater S (2004) The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnol Oceanogr 49:1713–1721

    Article  Google Scholar 

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

    Article  Google Scholar 

  46. Sand-Jensen K, Pedersen NL, Sondergaard M (2007) Bacterial metabolism in small temperate streams under contemporary and future climates. Freshw Biol 52:2340–2353

    Article  Google Scholar 

  47. Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1992) Wood decomposition over a first-order watershed: mass loss as a function of lignocellulase activity. Soil Biol Biochem 24:743–749

    Article  CAS  Google Scholar 

  48. Sinsabaugh RL, Antibus RK, Linkins AE, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593

    Article  CAS  Google Scholar 

  49. Sinsabaugh RL, Findlay S, Franchini P, Fischer D (1997) Enzymatic analysis of riverine bacterioplankton production. Limnol Oceanogr 42:29–38

    Article  CAS  Google Scholar 

  50. Sinsabaugh RL, Follstad Shah JJ (2010) Integrating resource utilization and temperature in metabolic scaling of riverine bacterial production. Ecology 91:1455–1465

    Article  PubMed  Google Scholar 

  51. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    Article  CAS  PubMed  Google Scholar 

  52. Smith EM, Prairie YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49:137–147

    Article  CAS  Google Scholar 

  53. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University, Princeton

    Google Scholar 

  54. Su R, Amonette R, Kuehn KA, Sinsabaugh RL, Neely RK (2007) Microbial dynamics associated with decaying Typha angustifolia litter in two contrasting Lake Erie coastal wetlands. Aquat Microb Ecol 46:295–307

    Article  Google Scholar 

  55. Thelaus J, Haecky P, Forsman M, Andersson A (2008) Predation pressure on bacteria increases along aquatic productivity gradients. Aquat Microb Ecol 52:45–55

    Article  Google Scholar 

  56. Thompson A, Sinsabaugh RL (2000) Matric and particulate phosphatase and leucine aminopeptidase activity in limnetic biofilms. Aquat Microb Ecol 21:151–159

    Article  Google Scholar 

  57. Tsuchiya Y, Ikenaga M, Kurniawan A, Hiraki A, Arakawa T, Kusakabe R, Morisaki H (2009) Nutrient-rich microhabitats within biofilms are synchronized with the external environment. Microbes Environ 24:43–51

    Article  Google Scholar 

  58. Van Horn DJ, Sinsabaugh RL, Dahm CN, Vesbach CD, Mitchell KR (2010) Linear and nonlinear responses of stream biofilm communities to a resource gradient. submitted

  59. Vargas CA, Martinez RA, Cuevas LA, Pavez MA, Cartes C, Gonzalez HE, Escribano R, Daneri G (2007) The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnol Oceanogr 52:1495–1510

    Google Scholar 

  60. Vrede K, Heldal M, Norland S, Bratbak G (2002) Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol 68:2965–2971

    Article  CAS  PubMed  Google Scholar 

  61. Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182:2675–2679

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

J.J.F.S. was supported by the National Science Foundation (DBI-0630558). R.L.S. was supported by the NSF EaGER program.

Author information

Authors and Affiliations

  1. Biology Department, University of New Mexico, Albuquerque, NM, 87131, USA

    Robert L. Sinsabaugh & David J. Van Horn

  2. Biology Department, Duke University, Durham, NC, 277081, USA

    Jennifer J. Follstad Shah

  3. Cary Institute of Ecosystem Studies, Millbrook, NY, USA

    Stuart Findlay

Authors
  1. Robert L. Sinsabaugh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David J. Van Horn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer J. Follstad Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stuart Findlay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert L. Sinsabaugh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sinsabaugh, R.L., Van Horn, D.J., Follstad Shah, J.J. et al. Ecoenzymatic Stoichiometry in Relation to Productivity for Freshwater Biofilm and Plankton Communities. Microb Ecol 60, 885–893 (2010). https://doi.org/10.1007/s00248-010-9696-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9696-4

Keywords

Search

Navigation