Microbial Ecology

, Volume 65, Issue 1, pp 1–11 | Cite as

Impaired Leaf Litter Processing in Acidified Streams

Learning from Microbial Enzyme Activities
  • Hugues Clivot
  • Michael Danger
  • Christophe Pagnout
  • Philippe Wagner
  • Philippe Rousselle
  • Pascal Poupin
  • François Guérold
Microbiology of Aquatic Systems

Abstract

Anthropogenic acidification in headwater streams is known to affect microbial assemblages involved in leaf litter breakdown. Far less is known about its potential effects on microbial enzyme activities. To assess the effects of acidification on microbial activities associated with decaying leaves, a 70-day litter bag experiment was conducted in headwater streams at six sites across an acidification gradient. The results revealed that microbial leaf decomposition was strongly and negatively correlated with total Al concentrations (r = −0.99, p < 0.001) and positively correlated with Ca2+ concentrations (r = 0.94, p = 0.005) and pH (r = 0.93, p = 0.008). Denaturing gradient gel electrophoresis analyses showed that microbial assemblages differed between non-impacted and impacted sites, whereas fungal biomass associated with decaying leaves was unaffected. The nutrient content of leaf detritus and ecoenzymatic activities of carbon (C), nitrogen (N) and phosphorus (P) acquisition revealed that N acquisition was unaltered, while P acquisition was significantly reduced across the acidification gradient. The P content of leaf litter was negatively correlated with total Al concentrations (r = −0.94, p < 0.01) and positively correlated with decomposition rates (r = 0.95, p < 0.01). This potential P limitation of microbial decomposers in impacted sites was confirmed by the particularly high turnover activity for phosphatase and imbalanced ratios between the ecoenzymatic activities of C and P acquisition. The toxic form of Al has well-known direct effects on aquatic biota under acidic conditions, but in this study, Al was found to also potentially affect microbially mediated leaf processing by interfering with the P cycle. These effects may in turn have repercussions on higher trophic levels and whole ecosystem functioning.

References

  1. 1.
    Arsuffi TL, Suberkropp K (1988) Effects of fungal mycelia and enzymatically degraded leaves on feeding and performance of Caddisfly (Trichoptera) larvae. J N Am Bentholl Soc 7:205–211CrossRefGoogle Scholar
  2. 2.
    Bärlocher F (2005) Leaf mass loss estimated by litter bag technique. In: Graça M, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition. Springer, Dordrecht, pp 37–42CrossRefGoogle Scholar
  3. 3.
    Bärlocher F, Kendrick B (1981) The role of aquatic hyphomycetes in the trophic structure of streams. In: Wicklow DT, Carroll GC (eds) The fungal community. Marcel Dekker, New York, pp 743–760Google Scholar
  4. 4.
    Baudoin JM, Guérold F, Felten V, Chauvet E, Wagner P, Rousselle P (2008) Elevated Aluminium concentration in acidified headwater streams lowers aquatic hyphomycete diversity and impairs leaf-litter breakdown. Microb Ecol 56:260–269PubMedCrossRefGoogle Scholar
  5. 5.
    Bittl T, Vrba J, Nedoma J, Kopácek J (2001) Impact of ionic aluminium on extracellular phosphatases in acidified lakes. Environ Microbiol 3:578–587PubMedCrossRefGoogle Scholar
  6. 6.
    Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  7. 7.
    Chamier AC (1987) Effect of pH on microbial degradation of leaf litter in seven streams of the English Lake District. Oecologia 71:491–500CrossRefGoogle Scholar
  8. 8.
    Chamier AC, Dixon PA (1982) Pectinases in leaf degradation by aquatic hyphomycetes: the enzymes and leaf maceration. J Gen Microbiol 128:2469–2483Google Scholar
  9. 9.
    Chamier AC, Tipping E (1997) Effects of aluminium in acid streams on growth and sporulation of aquatic hyphomycetes. Environ Pollut 96:289–298PubMedCrossRefGoogle Scholar
  10. 10.
    Dangles O, Chauvet E (2003) Effects of stream acidification on fungal biomass in decaying beech leaves and leaf palatability. Water Res 37:533–538PubMedCrossRefGoogle Scholar
  11. 11.
    Dangles O, Guérold F (1998) Influence of shredders in mediating breakdown rates of beech leaves in circumneutral and acidic forest streams. Arch Hydrobiol 151:649–666Google Scholar
  12. 12.
    Dangles O, Gessner MO, Guérold F, Chauvet E (2004) Impacts of stream acidification on litter breakdown: implications for assessing ecosystem functioning. J Appl Ecol 41:365–378CrossRefGoogle Scholar
  13. 13.
    Dangles O, Guérold F (2001) Linking shredders and leaf litter processing: insights from an acidic stream study. Int Rev Hydrobiol 86:395–406CrossRefGoogle Scholar
  14. 14.
    Duarte S, Cássio F, Pascoal C (2012) Denaturing Gradient Gel Electrophoresis (DGGE) in microbial ecology — Insights from freshwaters. In: Magdeldin S (ed) Gel electrophoresis — principles and basics. InTech, Rijeka, Croatia, pp 173–195Google Scholar
  15. 15.
    Duarte S, Pascoal C, Alves A, Correia A, Cássio F (2008) Copper and zinc mixtures induce shifts in microbial communities and reduce leaf litter decomposition in streams. Freshw Biol 53:91–101Google Scholar
  16. 16.
    Elwood JW, Newbold JD, Trimble AF, Stark RW (1981) The limiting role of phosphorus in a woodland stream ecosystem: effects of P enrichment on leaf decomposition and primary producers. Ecology 62:146–158CrossRefGoogle Scholar
  17. 17.
    Ely DT, Schiller DV, Valett HM (2010) Stream acidification increases nitrogen uptake by leaf biofilms: implications at the ecosystem scale. Freshw Biol 55:1337–1348CrossRefGoogle Scholar
  18. 18.
    Findlay SEG, Arsuffi TL (1989) Microbial growth and detritus transformations during decomposition of leaf litter in a stream. Freshw Biol 21:261–269CrossRefGoogle Scholar
  19. 19.
    Gessner MO, Chauvet E (2002) A case for using litter breakdown to assess functional stream integrity. Ecol Appl 12:498–510CrossRefGoogle Scholar
  20. 20.
    Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol 59:502–507PubMedGoogle Scholar
  21. 21.
    Gessner MO, Chauvet E (1994) Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75:1807CrossRefGoogle Scholar
  22. 22.
    Gessner MO, Schmitt A (1996) Use of solid-phase extraction to determine ergosterol concentrations in plant tissue colonized by fungi. Appl Environ Microbiol 62:415–419PubMedGoogle Scholar
  23. 23.
    Grattan RM, Suberkropp K (2001) Effects of nutrient enrichment on Yellow Poplar leaf decomposition and fungal activity in streams. J N Am Bentholl Soc 20:33–43CrossRefGoogle Scholar
  24. 24.
    Griffith MB, Perry SA, Perry WB (1995) Leaf litter processing and exoenzyme production on leaves in streams of different pH. Oecologia 102:460–466CrossRefGoogle Scholar
  25. 25.
    Guérold F, Boudot J-P, Jacquemin G, Vein D, Merlet D, Rouiller J (2000) Macroinvertebrate community loss as a result of headwater stream acidification in the Vosges Mountains (N-E France). Biodivers Conserv 9:767–783CrossRefGoogle Scholar
  26. 26.
    Gulis V, Suberkropp K (2003) Effect of inorganic nutrients on relative contributions of fungi and bacteria to carbon flow from submerged decomposing leaf litter. Microb Ecol 45:11–19PubMedCrossRefGoogle Scholar
  27. 27.
    Harrop BL, Marks JC, Watwood ME (2009) Early bacterial and fungal colonization of leaf litter in Fossil Creek, Arizona. J N Am Bentholl Soc 28:383–396CrossRefGoogle Scholar
  28. 28.
    Heard RM, Sharpe WE, Carline RF, Kimmel WG (1997) Episodic acidification and changes in fish diversity in Pennsylvania headwater streams. Trans Am Fish Soc 126:977–984CrossRefGoogle Scholar
  29. 29.
    Hieber M, Gessner MO (2002) Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026–1038CrossRefGoogle Scholar
  30. 30.
    Jansson M, Persson G, Broberg O (1986) Phosphorus in acidified lakes: the example of Lake Gardsjon, Sweden. Hydrobiologia 139:81–96CrossRefGoogle Scholar
  31. 31.
    Jenkins CC, Suberkropp K (1995) The influence of water chemistry on the enzymatic degradation of leaves in streams. Freshw Biol 33:245–253CrossRefGoogle Scholar
  32. 32.
    Kellner H, Luis P, Buscot F (2007) Diversity of laccase-like multicopper oxidase genes in Morchellaceae: identification of genes potentially involved in extracellular activities related to plant litter decay. FEMS Microbiol Ecol 61:153–163PubMedCrossRefGoogle Scholar
  33. 33.
    Kopácek J, Hejzlar J, Borovec J, Porcal P, Kotorova I (2000) Phosphorus inactivation by aluminum in the water column and sediments: lowering of in-lake phosphorus availability in an acidified watershed–lake ecosystem. Limnol Oceanogr 45:212–225CrossRefGoogle Scholar
  34. 34.
    Legendre P, Legendre L (1998) Numerical ecology. Developments in environmental modelling. Elsevier, AmsterdamGoogle Scholar
  35. 35.
    Meegan SK, Perry SA, Perry WB (1996) Detrital processing in streams exposed to acidic precipitation in the Central Appalachian Mountains. Hydrobiologia 339:101–110CrossRefGoogle Scholar
  36. 36.
    Mulholland PJ, Driscoll CT, Elwood JW, Osgood MP, Palumbo AV, Rosemond AD, Smith ME, Schofield C (1992) Relationships between stream acidity and bacteria, macroinvertebrates, and fish: a comparison of north temperate and south temperate mountain streams, USA. Hydrobiologia 239:7–24CrossRefGoogle Scholar
  37. 37.
    Mulholland PJ, Palumbo AV, Elwood JW, Rosemond AD (1987) Effects of acidification on leaf decomposition in streams. J N Am Benthol Soc 6:147–158CrossRefGoogle Scholar
  38. 38.
    Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing Gradient Gel Electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual, 3rd edn. Kluwer Academic Publishers, Dordrecht, pp 1–27, 3.4.4Google Scholar
  39. 39.
    Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedGoogle Scholar
  40. 40.
    Niyogi DK, Lewis WM, McKnight DM (2001) Litter breakdown in mountain streams affected by mine drainage: biotic mediation of abiotic controls. Ecol Appl 11:506–516CrossRefGoogle Scholar
  41. 41.
    Ormaza-González FI, Statham PJ (1996) A comparison of methods for the determination of dissolved and particulate phosphorus in natural waters. Water Res 30:2739–2747CrossRefGoogle Scholar
  42. 42.
    Oros-Sichler M, Gomes NCM, Neuber G, Smalla K (2006) A new semi-nested PCR protocol to amplify large 18S rRNA gene fragments for PCR-DGGE analysis of soil fungal communities. J Microbiol Methods 65:63–75PubMedCrossRefGoogle Scholar
  43. 43.
    Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microbiol 70:5266–5273PubMedCrossRefGoogle Scholar
  44. 44.
    Petersen RC, Cummins KW (1974) Leaf processing in a woodland stream. Freshw Biol 4:343–368CrossRefGoogle Scholar
  45. 45.
    Piña RG, Cervantes C (1996) Microbial interactions with aluminium. BioMetals 9:311–316PubMedCrossRefGoogle Scholar
  46. 46.
    R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
  47. 47.
    Romani A, Fischer H, Mille-Lindblom C, Tranvik L (2006) Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87:2559–2569PubMedCrossRefGoogle Scholar
  48. 48.
    Simon KS, Simon MA, Benfield EF (2009) Variation in ecosystem function in Appalachian streams along an acidity gradient. Ecol Appl 19:1147–1160PubMedCrossRefGoogle Scholar
  49. 49.
    Simpson KW, Bode RW, Colquhoun JR (1985) The macroinvertebrate fauna of an acid-stressed headwater stream system in the Adirondack Mountains, New York. Freshw Biol 15:671–681CrossRefGoogle Scholar
  50. 50.
    Sinsabaugh RL, Carreiro MM, Alvarez S (2002) Enzyme and microbial dynamics of litter decomposition. In: Burns RG, Dick RP (eds) Enzymes in the environment: Activity, ecology and applications. Marcel Dekker, New York, pp 249–265Google Scholar
  51. 51.
    Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  52. 52.
    Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798PubMedCrossRefGoogle Scholar
  53. 53.
    Sinsabaugh RL, Horn DJ, Follstad Shah JJ, Findlay S (2010) Ecoenzymatic stoichiometry in relation to productivity for freshwater biofilm and plankton communities. Microb Ecol 60:885–893PubMedCrossRefGoogle Scholar
  54. 54.
    Sridhar KR, Bärlocher F (2000) Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams. Appl Environ Microbiol 66:1114–1119PubMedCrossRefGoogle Scholar
  55. 55.
    Thompson PL, Bärlocher F (1989) Effect of pH on leaf breakdown in streams and in the laboratory. J N Am Bentholl Soc 8:203–210CrossRefGoogle Scholar
  56. 56.
    Zar JH (1999) Biostatistical analysis. Prentice Hall, Englewood CliffsGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Hugues Clivot
    • 1
    • 2
  • Michael Danger
    • 1
    • 2
  • Christophe Pagnout
    • 1
    • 2
  • Philippe Wagner
    • 1
    • 2
  • Philippe Rousselle
    • 1
    • 2
  • Pascal Poupin
    • 1
    • 2
  • François Guérold
    • 1
    • 2
  1. 1.Université de LorraineLaboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE), UMR 7146MetzFrance
  2. 2.CNRSLaboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE), UMR 7146MetzFrance

Personalised recommendations