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Isolation, Characterization and Practical Significance of Cellulose Degrading Bacteria from the Gut Wall of Two Ecologically Distinct Earthworms


Affiliations
1 Department of Plant and Environmental Protection Sciences, University of Hawaii, 3190 Maile Way, Honolulu, HI, 96822, United States
2 Division of Life Sciences, Institute of Advanced Study in Science and Technology, DST (GoI), Paschim Boragaon, Guwahati 781 035, India
3 School of Natural Resource Management, College of Post Graduate Studies, Central Agricultural University (Imphal), Umiam 793 103, India
 

This study has determined the relationship of cultur-able community of cellulose degrading bacteria (CDB) within the gut walls of two habitat-specific earthworm species, epigeic (compost heap inhabitant) earthworm, Perionyx excavatus (PE) and an endogeic (submerged rice field inhabitant), Glyphidrilus spelaeotes (GS) and their functional significance. The 16Sr RNA analysis for the isolated CDB from two ecologically distinct earthworms clearly showed the presence of distinct communities of CDB in their gut ecosystem. Enzymatic assay of cellulase for the isolated CDB showed sig-nificantly higher cellulase activity compared to the reference strain M-23, Cellulomonas cellulans (P < 0.01, one-way ANOVA). The functional signifi-cance of such high cellulase activity was also demon-strated by the enhancement of decomposition of rice straw and fresh vegetation biomass in the presence of native microbiota community. The growth rate of CDB of epigeic PE was approximately twice slower than that of CDBs of endogeic GS. The CDB of PE exhibited 12 polymorphs of esterase isozyme as against 4 polymorphs for CDB of GS. The present study emphasizes the functionally significant relation-ship of gut wall CDB and host earthworm for sustaining efficient C-cycling in agroecosystems.

Keywords

Cellulase Activity, Easterase Isozyme, Earthworm–Microorganism Interactions, Glyphidrilus spelaeotes, Intestinal Microbiology, Soil Fauna.
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  • Jones, C. G., Lawton, J. H. and Shachak, M., Organisms as Eco-system Engineers, in Ecosystem Management, Springer, 1996, pp. 130–147.
  • Brown, G. G., Barois, I. and Lavelle, P., Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur. J. Soil Biol., 2000, 36(3), 177–198.
  • Furlong, M. A. et al., Molecular and culture-based analyses of prokaryotic communities from an agricultural soil and the burrows and casts of the earthworm Lumbricus rubellus. Appl. Environ. Microbiol., 2002, 68(3), 1265–1279.
  • Schonholzer, F., Hahn, D. and Zeyer, J., Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol. Ecol., 1999, 28(3), 235–248.
  • Ihssen, J. et al., N2O-producing microorganisms in the gut of the earthworm Aporrectodea caliginosa are indicative of ingested soil bacteria. Appl. Environ. Microbiol., 2003, 69(3), 1655–1661.
  • Schramm, A. et al., Acidovorax-like symbionts in the nephridia of earthworms. Environ. Microbiol., 2003, 5(9), 804–809.
  • Singleton, D. R. et al., Identification of uncultured bacteria tightly associated with the intestine of the earthworm Lumbricus rubellus (Lumbricidae; Oligochaeta). Soil Biol. Biochem., 2003, 35(12), 1547–1555.
  • Egert, M. et al., Molecular profiling of 16S rRNA genes reveals diet-related differences of microbial communities in soil, gut, and casts of Lumbricus terrestris L.(Oligochaeta: Lumbricidae). FEMS Microbiol. Ecol., 2004, 48(2), 187–197.
  • Knapp, B. et al., Application of denaturing gradient gel electrophoresis for analysing the gut microflora of Lumbricus rubellus Hoffmeister under different feeding conditions. Bull. Entomol. Res., 2008, 98(03), 271–279.
  • Lattaud, C. et al., Activities of the digestive enzymes in the gut and in tissue culture of a tropical geophagous earthworm, Polypheretima elongata (Megascolecidae). Soil Biol. Biochem., 1997, 29(3), 335–339.
  • Thakuria, D. et al., Gut wall bacteria in earthworms: a natural selection process. ISME J., 2010, 4, 357–366.
  • Howath, W., Carbon cycling and formation of soil organic matter. In Soil Microbiology, Ecology and Biochemistry (ed. Paul, E. A.), Academic Press, Canada, 2007, 3rd edn, pp. 303–339.
  • Goswami, C. and Talukdar, N. C., In-situ mineralization of ahu rice stubble and its effect on succeeding rice and soil properties. In Biotechnology in Sustainable and Organic Farming, Shree Publishers, 2004, pp. 313–317.
  • Chanabun, R., Sutcharit, C., Tongkerd, P. and Panha, S., The semi-aquatic freshwater earthworms of the genus Glyphidrilus Horst, 1889 from Thailand (Oligochaeta, Almidae) with redescriptions of several species. ZooKeys, 2013, 265, I-76; doi:10.3897/zookeys. 2653911, p. 1–74.
  • Vijayamohanan, Occurrence and density of earthworm in relation to soil factors and altitudes in Kollan district, Kerela. Final Project Report to University Grants Commission, India, 2014, p. 20; www.bjmgovtcollege.in
  • Thakuria, D. et al., Field preservation and DNA extraction meth-ods for intestinal microbial diversity analysis in earthworms. J. Microbiol. Meth., 2009, 76(3), 226–233.
  • SubbaRao, N. S., Soil Microbiology Fourth Edition of Soil Micro-organisms and Plant Growth, Oxford & IBH, New Delhi, 1999, p. 407.
  • Cremer, A., Antibiotic Sensitivity and Assay Tests, Butterworth, London, 1980, p. 521.
  • Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970, 227(5259), 680–685.
  • Lane, D. J., 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. and Good-fellow, M.), John Wiley, Chichester, United Kingdom, 1991, pp. 115–175.
  • Zhang, W., Dunkle, J. A. and Cate, J. H. D., Structures of the ribosome in intermediate states of ratcheting. Science, 2009, 325(5943), 1014–1017.
  • Sambrook, J. and Russell David, W., Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, 1989, p. 3.
  • Magurran, A. E., Measuring biological diversity. Afr. J. Aquatic Sci., 2004, 29(2), 285–286.
  • Bray, J. R. and Curtis, J. T., An ordination of the upland forest communities of southern Wisconsin. Ecol. Monographs, 1957, 27(4), 325–349.
  • Clarke, K. R., Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol., 1993, 18, 117.
  • Hallatt, L., Viljoen, S. and Reinecke, A., Moisture requirements in the life cycle of Perionyx excavatus (Oligochaeta). Soil Biol. Bio-chem., 1992, 24(12), 1333–1340.
  • Goullet, P. and Picard, B., The electrophoretic polymorphism of bacterial esterases. FEMS Microbiol. Rev., 1995, 16(1), 7–31.
  • Kudo, H., Cheng, K.-J. and Costerton, J., Electron microscopic study of the methylcellulose-mediated detachment of cellulolytic rumen bacteria from cellulose fibers. Can. J. Microbiol., 1987, 33(3), 267–272.
  • Mandels, M. and Weber, J, Physical structure of cellulose. Adv. Chem. Ser., 1969, 96, 391.
  • Garg, S. and Neelakantan, S., Studies on the properties of cellulase enzyme from Aspergillus terreus GN1. Biotechnol. Bioeng., 1982, 24(3), 737–742.
  • Mandels, M. et al., Enzymatic hydrolysis of cellulose: evaluation of cellulase culture filtrates under use conditions. Biotechnol. Bio-eng., 1981, 23(9), 2009–2026.
  • Valle-Molinares, R., Borges, S. and Rios-Velazquez, C., Charac-terization of possible symbionts in Onychochaeta borincana (Annelida: Glossoscolecidae). Eur. J. Soil Biol., 2007, 43, S14–S18.
  • Knapp, B. et al., Diet-related composition of the gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning. Soil Biol. Biochem., 2009, 41(11), 2299–2307.

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  • Isolation, Characterization and Practical Significance of Cellulose Degrading Bacteria from the Gut Wall of Two Ecologically Distinct Earthworms

Abstract Views: 319  |  PDF Views: 87

Authors

Kishore K. Dey
Department of Plant and Environmental Protection Sciences, University of Hawaii, 3190 Maile Way, Honolulu, HI, 96822, United States
Narayan C. Talukdar
Division of Life Sciences, Institute of Advanced Study in Science and Technology, DST (GoI), Paschim Boragaon, Guwahati 781 035, India
Fenella M. W. Nongkhlaw
School of Natural Resource Management, College of Post Graduate Studies, Central Agricultural University (Imphal), Umiam 793 103, India
Dwipendra Thakuria
School of Natural Resource Management, College of Post Graduate Studies, Central Agricultural University (Imphal), Umiam 793 103, India

Abstract


This study has determined the relationship of cultur-able community of cellulose degrading bacteria (CDB) within the gut walls of two habitat-specific earthworm species, epigeic (compost heap inhabitant) earthworm, Perionyx excavatus (PE) and an endogeic (submerged rice field inhabitant), Glyphidrilus spelaeotes (GS) and their functional significance. The 16Sr RNA analysis for the isolated CDB from two ecologically distinct earthworms clearly showed the presence of distinct communities of CDB in their gut ecosystem. Enzymatic assay of cellulase for the isolated CDB showed sig-nificantly higher cellulase activity compared to the reference strain M-23, Cellulomonas cellulans (P < 0.01, one-way ANOVA). The functional signifi-cance of such high cellulase activity was also demon-strated by the enhancement of decomposition of rice straw and fresh vegetation biomass in the presence of native microbiota community. The growth rate of CDB of epigeic PE was approximately twice slower than that of CDBs of endogeic GS. The CDB of PE exhibited 12 polymorphs of esterase isozyme as against 4 polymorphs for CDB of GS. The present study emphasizes the functionally significant relation-ship of gut wall CDB and host earthworm for sustaining efficient C-cycling in agroecosystems.

Keywords


Cellulase Activity, Easterase Isozyme, Earthworm–Microorganism Interactions, Glyphidrilus spelaeotes, Intestinal Microbiology, Soil Fauna.

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DOI: https://doi.org/10.18520/cs%2Fv114%2Fi07%2F1474-1484