Abstract
Cellulose is the most abundant polymer in nature and constitutes a large pool of carbon for microorganisms, the main agents responsible for soil organic matter decomposition. Cellulolysis occurs as the result of the combined action of fungi and bacteria with different requirements. Earthworms influence decomposition indirectly by affecting microbial population structure and dynamics and also directly because the guts of some species possess cellulolytic activity. Here we assess whether the earthworm Eisenia fetida (Savigny 1826) digests cellulose directly (i.e., with its associated gut microbiota) and also whether the effects of E. fetida on microbial biomass and activity lead to a change in the equilibrium between fungi and bacteria. By enhancing fungal communities, E. fetida would presumably trigger more efficient cellulose decomposition. To evaluate the role of E. fetida in cellulose decomposition, we carried out an experiment in which pig slurry, a microbial-rich substrate, was treated in small-scale vermireactors with and without earthworms. The presence of earthworms in vermireactors significantly increased the rate of cellulose decomposition (0.43 and 0.26% cellulose loss day−1, with and without earthworms, respectively). However, the direct contribution of E. fetida to degradation of cellulose was not significant, although its presence increased microbial biomass (Cmic) and enzyme activity (cellulase and β-glucosidase). Surprisingly, as fungi may be part of the diet of earthworms, the activity of E. fetida triggered fungal growth during vermicomposting. We suggest that this activation is a key step leading to more intense and efficient cellulolysis during vermicomposting of organic wastes.
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References
Atalla, RH, Hackney, JM, Uhlin, I, Thompson, NS (1993) Hemicelluloses as structure regulators in the aggregation of native cellulose. Int J Biol Macromol 15: 109–112
Benitez, E, Sainz, H, Nogales, R (2005) Hydrolytic enzyme activities of extracted humic substances during the vermicomposting of a lignocellulosic olive waste. Bioresour Technol 96: 785–790
Brown, GG, Doube, BM (2004) Functional interactions between earthworms, microorganisms, organic matter, and plants. In: Edwards, CA (Ed.) Earthworm Ecology, 2nd ed. CRC Press, Boca Raton, pp 213–224
Cooke, A (1983) The effects of fungi on food selection by Lumbricus terrestris L. In: Satchell, JE (Ed.) Earthworm Ecology, Chapman & Hall, London, pp 365–373
de Boer, W, Folman, LB, Summerbell, RC, Boddy, L (2004) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795–811
Domínguez, J (2004) State of the art and new perspectives in vermicomposting research. In: Edwards, CA (Ed.) Earthworm Ecology, 2nd ed. CRC Press, Boca Raton, pp 401–425
Edwards, CA (2004) Earthworm Ecology, 2nd ed. CRC Press, Boca Raton
Eivazi, F, Tabatabai, MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20: 601–606
Fischer, K, Hahn, D, Amann, RI, Daniel, O, Zeyer, J (1995) In situ analysis of the bacterial community in the gut of the earthworm Lumbricus terrestris L., by whole-cell hybridization. Can J Microbiol 41: 666–673
Garrett, SD (1981) Soil Fungi and Soil Fertility. Pergamon Press, Oxford
Goering, HK, Van Soest, PJ (1970) Forage Fiber Analysis, Agr. Handbook No. 379. Agricultural Research Service, USDA, Washington, DC
Goyal, A, Ghosh, B, Eveleigh, D (1991) Characteristics of fungal cellulases. Bioresour Technol 36: 37–50
Hatanaka, K, Ishioka, Y, Furuichi, E (1983) Cultivation of Eisenia fetida using dairy waste sludge cake. In: Satchell, JE (Ed.) Earthworm Ecology from Darwin to Vermiculture, Chapman and Hall, London, pp 323–329
Hayano, K (1986) Cellulase complex in tomato field soil: induction, localization and some properties. Soil Biol Biochem 18: 215–219
Hayano, K, Tubakil, P (1985) Origin and properties of β-glucosidase activity of tomato-field soil. Soil Biol Biochem 17: 553–557
Haynes, RJ, Fraser, PM, Piercy, JE, Tregurtha, RJ (2003) Casts of Aporrectodea caliginosa (Savigny) and Lumbricus rubellus (Hoffmeister) differ in microbial activity, nutrient availability and aggregate stability. Pedobiologia 47: 882–887
Hu, S, van Bruggen, AHC (1997) Microbial dynamics associated with multiphasic decomposition of 14C-labelled cellulose in soil. Microb Ecol 33: 134–143
Klamer, M, Baath, E (2004) Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PFLA 18:2ω6,9. Soil Biol Biochem 36: 57–65
Kristufek, V, Ravasz, K, Pizl, V (1992) Changes in densities of bacteria and microfungi during gut transit in Lumbricus rubellus and Aporrectodea caliginosa (Oligochaeta: Lumbricidae). Soil Biol Biochem 12: 1499–1500
Lattaud, C, Locati, S, Mora, P, Rouland, C (1997a) Origin and activities of glycolytic enzymes in the gut of the tropical geophagous earthworm Millsonia anomala from Lamto (Cote d'Ivoire). Pedobiologia 41: 242–251
Lattaud, C, Zhang, BG, Locati, S, Rouland, C, Lavelle, P (1997b) Activities of the digestive enzymes in the gut and in tissue culture of a tropical geophagous earthworm, Polipheretima elongata (Megascolecidae). Soil Biol Biochem 29: 335–339
Lavelle, P, Spain, AV (2001) Soil Ecology. Kluwer Academic Publishers, London
Leschine, SB (1995) Cellulose degradation in anaerobic environments. Annu Rev Microbiol 49: 399–426
Loquet, M, Vinceslas, M (1987) Cellulolyse et ligninolyse liées au tube digestif d'Eisenia fetida andrei Bouché. Rev Ecol Biol Sol 24: 559–571
Lynd, LR, Weimer, PJ, van Zyl, WH, Pretorius, IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66: 506–577
McCarthy, AJ, Williams, ST (1992) Actinomycetes as agents of biodegradation in the environment—a review. Gene 115: 189–192
Moody, SA, Briones, MJI, Pierce, TG, Dighton, J (1995) Selective consumption of decomposing wheat straw by earthworms. Soil Biol Biochem 27: 1209–1213
Nodar, R, Acea, MJ, Carballas, T (1992) Poultry slurry microbial population: composition and evolution during storage. Biores Technol 40: 29–34
Pižl, V, Novakova, A (2003) Interactions between microfungi and Eisenia andrei (Oligochaeta) during cattle manure vermicomposting. Pedobiologia 47: 895–899
Potvin, C, Lechowicz, MJ, Tardif, S (1990) The statistical analysis of ecological response curves obtained from experiments involving repeated measures. Ecology 71: 1389–1400
Richmond, PA (1991) Occurrence and functions of native cellulose. In: Haigler, CH, Weimer, JP (Eds.) Biosynthesis and Biodegradation of Cellulose. Dekker, New York, pp 5–23
Saito, M, Wada, H, Takay, Y (1990) Development of a microbial community on cellulose buried in waterlogged soil. Biol Fertil Soils 9: 301–305
Salinitro, JP, Blake, IG, Muirhead, PA (1977) Isolation and identification of faecal bacteria from adult swine. Appl Environ Microbiol 33: 79–84
Scheu, S (1993) Cellulose and lignin decomposition in soils from different ecosystems on limestone as affected by earthworm processing. Pedobiologia 37: 167–177
Schinner, F, Von Mersi, W (1990) Xylanase-, CM-cellulase- and invertase activity in soil: an improved method. Soil Biol Biochem 22: 511–515
Schönholzer, F, Hahn, D, Zeyer, J (1999) Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol Ecol 28: 235–248
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
Sinsabaugh, RL, Linkins, AE (1988) Adsorption of cellulase components by leaf litter. Soil Biol Biochem 20: 927–931
Sinsabaugh, RL, Linkins, AE (1993) Statistical modelling of litter decomposition from integrated cellulase activity. Ecology 74: 1594–1597
Tiunov, A, Scheu, S (2000) Microfungal communities in soil, litter and casts of Lumbricus terrestris L. (Lumbricidae): a laboratory experiment. Appl Soil Ecol 14: 17–26
Tiunov, AV, Scheu, S (2004) Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138: 83–90
Urbásek, F, Pižl, V (1991) Activity of digestive enzymes in the gut of five earthworm species (Oligochaeta: Lumbricidae). Rev Ecol Biol Sol 28: 461–468
Vance, ED, Brookes, PC, Jenkinson, DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19: 703–707
Vinceslas-Akpa, M, Loquet, M (1997) Organic matter transformations in lignocellulosic waste products composted or vermicomposted (Eisenia fetida andrei): chemical analysis and 13C CPMAS NMR spectroscopy. Soil Biol Biochem 29: 751–758
von Ende, CN (2001) Repeated-measures analysis. In: Scheiner, SM, Gurevitch, J (Eds.) Design and Analysis of Ecological Experiments, Oxford University Press, pp 134–157
Whitehead, TR, Cotta, MA (2001) Characterisation and comparison of microbial populations in swine faeces and manure storage pits by 16S rDNA gene sequence analyses. Anaerobe 7: 181–187
Young, JC (1995) Microwave-assisted extraction of the fungal metabolite ergosterol and total fatty acids. J Agric Food Chem 43: 2904–2910
Zhang, BG, Li, GT, Shen, TS, Wang, JK, Sun, Z (2000) Changes in microbial biomass C, N and P and enzyme activities in soil incubated with the earthworms Metaphire guillelmi or Eisenia fetida. Soil Biol Biochem 32: 2055–2062
Zhang, BG, Rouland, C, Lattaud, C, Lavelle, P (1993) Activity and origin of digestive enzymes in the gut of tropical earthworm Pontoscolex corethurus. Eur J Soil Biol 29: 7–11
Zhu, J (2000) A review of microbiology in swine manure odor control. Agric Ecosyst Environ 78: 93–106
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This research was supported by CICYT (AGL2003-01570) and Xunta de Galicia (PGIDIT03PXIB30102PR) grants.
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Aira, M., Monroy, F. & Domínguez, J. Eisenia fetida (Oligochaeta, Lumbricidae) Activates Fungal Growth, Triggering Cellulose Decomposition During Vermicomposting. Microb Ecol 52, 738–747 (2006). https://doi.org/10.1007/s00248-006-9109-x
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DOI: https://doi.org/10.1007/s00248-006-9109-x