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Use of Terminal Restriction Length Polymorphism (T-RFLP) Analysis to Evaluate Uncultivable Microbial Community Structure of Soil
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 Title & Authors
Use of Terminal Restriction Length Polymorphism (T-RFLP) Analysis to Evaluate Uncultivable Microbial Community Structure of Soil
Chauhan, Puneet Singh; Shagol, Charlotte C.; Yim, Woo-Jong; Tipayno, Sherlyn C.; Kim, Chang-Gi; Sa, Tong-Min;
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Various environmental ecosystems are valuable sources for microbial ecology studies, and their analyses using recently developed molecular ecological approaches have drawn significant attention within the scientific community. Changes in the microbial community structures due to various anthropogenic activities can be evaluated by various culture-independent methods e.g. ARISA, DGGE, SSCP, T-RFLP, clone library, pyrosequencing, etc. Direct amplification of total community DNA and amplification of most conserved region (16S rRNA) are common initial steps, followed by either fingerprinting or sequencing analysis. Fingerprinting methods are relatively quicker than sequencing analysis in evaluating the changes in the microbial community. Being an efficient, sensitive and time- and cost effective method, T-RFLP is regularly used by many researchers to access the microbial diversity. Among various fingerprinting methods T-RFLP became an important tool in studying the microbial community structure because of its sensitivity and reproducibility. In this present review, we will discuss the important developments in T-RFLP methodology to distinguish the total microbial diversity and community composition in the various ecosystems.
Microbial diversity;Community structure;T-RFLP;16S rRNA;
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T-RFLP analysis of soil bacterial structure from Cerrado within the Sete Cidades National Park, Brazil, Neotropical Biodiversity, 2016, 2, 1, 163  crossref(new windwow)
Abdo, Z., U.M., Schutte, S.J. Bent, C.J. Williams, L.J. Forney, and P. Joyce. 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ. Microbiol. 8:929-938. crossref(new window)

Abell, G.C., A.T. Revill, C. Smith, A.P. Bissett, J.K. Volkman, and S.S. Robert. 2010. Archaeal ammonia oxidizers and nirStype denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J. 4:286-300. crossref(new window)

Acinas, S.G., L.A. Marcelino, V. Klepac-Ceraj, and M.F. Ploz. 2004. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 168:2629-2635.

Amann, R.I., W. Ludwig, and K. Schleifer. 1995. Phlyogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.

Anderson, I.C., B.A. Bastias, D.R. Genney, P.I. Parkin, and J.W. Cairney. 2007. Basidiomycete fungal communities in Australian sclerophyll forest soil are altered by repeated prescribed burning. Mycol. Res. 111:482-486. crossref(new window)

Ayala-del-Rio, H.L., S.J. Callister, C.S. Criddle, and J.M. Tiedje. 2004. Correspondence between community structure and function during succession in phenol- and phenol-plustrichloroethene-fed sequencing batch reactors. Appl. Environ. Microbiol. 70:4950-4960. crossref(new window)

Becker, R., P. Boger, R. Oehlmann, and A. Ernst. 2000. PCR bias in ecological analysis: a case study for quantitative Taq nuclease assays in analyses of microbial communities. Appl. Environ. Microbiol. 66:4945-4953. crossref(new window)

Becker, R., U. Behrendt, B. Hommel, S. Kropf, and A. Ulrich. 2008. Effects of transgenic fructan-producing potatoes on the community structure of rhizosphere and phyllosphere bacteria. FEMS Microbiol. Ecol. 66:411-425. crossref(new window)

Behr, S., M. Matzig, A. Levin, H. Eickhoff, and C. Heller. 1999. A fully automated multicapillary electrophoresis device for DNA analysis. Electrophoresis. 20:1492-1507. crossref(new window)

Bent, S.J. and L.J. Forney. 2008. The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J. 2:689-695. crossref(new window)

Berg, G., A. Krechel, M. Ditz, R.A. Sikora, A. Ulrich, and J. Hallmann. 2005. Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol. Ecol. 51:215-229. crossref(new window)

Blackwood, C.B., D. Huddleston, D.R. Zak, and J.S. Buyer. 2007. Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl. Environ. Microbiol. 73:5276-5283. crossref(new window)

Blaut, M., M.D. Collins, G.W. Welling, J. Dore, J. van Loo, and W. de Vos. 2002. Molecular biological methods for studying the gut microbiota: the EU human gut flora project. British J. Nut. 88:S203-S211.

Bowman, J.P. and R.D. McCuaig. 2003. Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl. Environ. Microbiol. 69:2463-2483. crossref(new window)

Braker, G., H.L. Ayala-del-Rio, A.H. Devol, A. Fesefeldt, and J.M. Tiedje. 2001. Community structure of denitrifiers, bacteria, and archaea along redox gradients in Pacific Northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl. Environ. Microbiol. 67:1893-1901. crossref(new window)

Brown, M.V., M.S. Schwalbach, I. Hewson, and J.A. Fuhrman. 2005. Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. Environ. Microbiol. 7:1466-1479 crossref(new window)

Brunk, C.F., E. Avaniss-Aghajani, and C.A. Brunk. 1996. A computer analysis of primer and probe hybridization potential with bacterial small-subunit rRNA sequences. Appl. Environ. Microbiol. 62:872-879.

Cadillo-Quiroz, H., J.B. Yavitt, S.H. Zinder, and J.E. Thies. 2009. Diversity and community structure of Archaea inhabiting the rhizoplane of two contrasting plants from an acidic bog. Microb. Ecol. 59:757-767.

Chan, O.C., X. Yang, Y. Fu, Z. Feng, L. Sha, P. Casper, and X. Zou. 2006. 16S rRNA gene analyses of bacterial community structures in the soils of evergreen broad-leaved forests in south-west China. FEMS Microbiol. Ecol. 58:247-259. crossref(new window)

Chen, Z., X. Luo, R. Hu, M. Wu, J. Wu, and W. Wei. 2010. Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb. Ecol. 60:850-861. crossref(new window)

Conn, V.M. and C.M. Franco. 2004. Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl. Environ. Microbiol. 70:1787-1794. crossref(new window)

Cordova-Kreylos, A.L., Y.P. Cao, P.G. Green, H.M. Hwang, K.M. Kuivila, M.G. LaMontagne, L.C. Van De Werfhorst, P.A. Holden, and K.M. Scow. 2006. Diversity, composition, and geographical distribution of microbial communities in california salt marsh sediments. Appl. Environ. Microbiol. 72:3357-3366. crossref(new window)

Crosby, L.D. and C.S. Criddle. 2003. Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques. 34:790-764.

Culman, S.W., J.M. Duxbury, T.G. Lauren, and J.E. Thies. 2006. Microbial community response to soil solarization in Nepal's rice-wheat cropping system. Soil Biol. Biochem. 38:3359-3371. crossref(new window)

daCJesus, E., T.L. Marsh, J.M. Tiedje, and F.M. deSMoreira. 2009. Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J. 3:1004-1011. crossref(new window)

Dedysh, S.V., T. Pankratov, S.E. Belova, I.S. Kulichevskaya, and W. Liesack. 2006. Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl. Environ. Microbiol. 72:2110-2117. crossref(new window)

Derakshani, M., T. Lukow, and W. Liesack. 2001. Novel bacterial lineages at the (sub) division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl. Environ. Microbiol. 67:623-631. crossref(new window)

Devare, M.H., C.M. Jones, and J.E. Thies. 2004. Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity, and diversity. J. Environ. Qual. 33:837-843. crossref(new window)

Dollhopf, S.L., S.A. Hashsham, and J.M. Tiedje. 2001. Interpreting 16S rDNA T-RFLP data: application of selforganizing maps and principal component analysis to describe community dynamics and convergence. Microb. Ecol. 42:495-505 crossref(new window)

Donis-Keller, H., A.M. Maxam, and W. Gilbert. 1977. Mapping adenines, guanines and pyrimidines in RNA. Nucleic Acids Res. 4:2527-2538. crossref(new window)

Duineveld, B.M., G.A. Kowalchuk, A. Keijzer, and J.D. van Elsas 2001. Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl. Environ. Microbiol. 67:172- 178. crossref(new window)

Dunbar, J., L.O. Ticknor, and C.R. Kuske. 2000. Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl. Environ. Microbiol. 66:2943-2950. crossref(new window)

Dunbar, J., L.O. Ticknor, and C.R. Kuske. 2001. Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl. Environ. Microbiol. 67:190-197. crossref(new window)

Dunbar, J., S.M. Barns, L.O. Ticknor, and C.R. Kuske. 2002. Empirical and theoretical bacterial diversity in four Arizona soils. App. Environ. Microbiol. 68:3035-3045. crossref(new window)

Eckburg P.B., E.M. Bik, C.N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S.R. Gill, K.E. Nelson, and D.A. Relman. 2005. Diversity of the human intestinal microbial flora. Science. 308:1635-1638. crossref(new window)

Egert, M. and M.W. Friedrich. 2003. Formation of pseudoterminal restriction fragments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69:2555-2562. crossref(new window)

Egert, M. and M.W. Friedrich. 2005. Post-amplification Klenow fragment treatment alleviates PCR bias caused by partially single-stranded amplicons. J. Microbiol. Meth. 61:69-75. crossref(new window)

Egert, M., S. Marhan, B. Wagner, S. Scheu, and M.W. Friedrich. 2004. 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. 48:187-197. crossref(new window)

Elshahed, M.S., F.Z. Najar, B.A. Roe, A. Oren, T.A. Dewers, and L.R. Krumholz. 2004. Survey of Archaeal diversity reveals an abundance of halophilic Archaea in low-salt, sulfide- and sulfur-rich spring. Appl. Environ. Microbiol. 70:2230-2239. crossref(new window)

Engebreston, J.J. and C.L. Moyer. 2003. Fidelity of select restriction endonucleases in determining microbial diversity by terminal-restriction fragment length polymorphism. Appl. Environ. Microbiol. 69:4823-4829. crossref(new window)

Ferrando, L. and S. Tarlera. 2009. Activity and diversity of methanotrophs in the soil-water interface and rhizospheric soil from a flooded temperate rice field. J. Appl. Microbiol. 106:306-316. crossref(new window)

Fierer, N., J.P. Schimel, and P.A. 2003. Holden. Influence of drying-rewetting frequency on soil bacterial community structure. Microb. Ecol. 45:63-71. crossref(new window)

Fisher, M.M. and E.W. Triplett. 1999 Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl. Environ. Microbiol. 65:4630-4636.

Flores-Mireles, A.L., S.C. Winans, and G. Holguin. 2007. Molecular characterization of diazotrophic and denitrifying bacteria associated with mangrove roots. Appl. Environ. Microbiol. 73:7308-7321. crossref(new window)

Franklin, R.B. and A.L. Mills. 2003. Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. FEMS Microbiol. Ecol. 44:335-346. crossref(new window)

Friedrich, M.W., D. Schmitt-Wagner, T. Lueders and A. Brune. 2001. Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil-feeding termite Cubitermes orthognathus. Appl. Environ. Microbiol. 67:4880-4890. crossref(new window)

Fuka, M.M., M. Engel, A. Hagn, J.C. Munch, M. Sommer, and M. Schloter. 2008. Changes of diversity pattern of proteolytic bacteria over time and space in an agricultural soil. Microb. Ecol. 57:391-401.

Garbeva, P., van Veen J.A., and J.D. van Elsas. 2004. Microbial diversity in soil: Selection of microbial populations by plant and soil type and implications for disease suppressiveness. Ann. Rev. Phytopathol. 42:243-70. crossref(new window)

Gauch, H.G. Jr. 1992. Statistical analysis of regional yield trials: AMMI analysis of factorial designs. Elsevier, Amsterdam, the Netherlands.

Ge, Y., J.P. Schimel, and P.A. Holden. 2011. Evidence for negative effects of $TiO_2$ and ZnO nanoparticles on soil bacterial communities. Environ. Sci. Technol. DOI: 10.1021/es103040t.

Genney, D.R., I.C. Anderson, and I.J. Alexander. 2006. Finescale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol. 170:381-390. crossref(new window)

Grant, R.J., L.M. Muckian, N.J.W. Clipson, and E.M. Doyle. 2007. Microbial community changes during the bioremediation of creosote-contaminated soil. Lett. Appl. Microbiol. 44:293-300. crossref(new window)

Grüter, D., B. Schmid, and H. Brandl. 2006. Influence of plant diversity and elevated atmospheric carbon dioxide levels on belowground bacterial diversity. BMC Microbiol. 6:68. crossref(new window)

Hackl, E., S. Zechmeister-Boltenstern, L. Bodrossy, and A. Sessitsch. 2004. Comparison of diversities and compositions of bacterial populations inhabiting natural forest soils. Appl. Environ. Microbiol. 70:5057-5065. crossref(new window)

Hahn, M., J. Wilhelm, and A. Pingoud. 2001. Influence of fluorophore dye labels on the migration behavior of polymerase chain reaction-amplified short tandem repeats during denaturing capillary electrophoresis. Electrophoresis. 22:2691-2700. crossref(new window)

Hein, J.W., G.V. Wolfe, and K.A. Blee. 2007. Comparison of rhizosphere bacterial communities in Arabidopsis thaliana mutants for systemic acquired resistance. Microb. Ecol. 55:333-343.

Hewson, I. and J.A. Fuhrman. 2006. Improved strategy for comparing microbial assemblage fingerprints. Microb. Ecol. 51:147-153. crossref(new window)

Hill, J.E., R.P. Seipp, M. Betts, L. Hawkins, A.G. Van Kessel, W.L. Crosby, and S.M. Hemmingsen. 2002. Extensive profiling of a complex microbial community by high-througput sequencing. Appl. Environ. Microbiol. 68:3055-3066. crossref(new window)

Hoffmann, T., H.P. Horz, D. Kemnitz, and R. Conrad. 2002. Diversity of the particulate methane monooxygenase gene in methanotrophic samples from different rice field soils in China and the Philippines. Syst. Appl. Microbiol. 25:267-274. crossref(new window)

Hopkins, M.J., R. Sharp, and G.T. Macfarlane. 2001. Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut. 48:198-205. crossref(new window)

Horz, H.P., J.H. Rotthauwe, T. Lukow, and W. Liesack. 2000. Identification of major subgroups of ammonia-oxidizing bacteria in environmental samples by T-RFLP analysis of amoA PCR products. J. Microbiol. Methods. 39:197-204. crossref(new window)

Hoshino, T., T. Terahara, K. Yamada, H. Okuda, I. Suzuki, S. Tsuneda, A. Hirata, and Y. Inamori. 2006. Long-term monitoring of the succession of a microbial community in activated sludge from a circulation flush toilet as a closed system. FEMS Microbiol. Ecol. 55:459-470. crossref(new window)

Hullar, M.A J., L.A. Kaplan, and D.A. Stahl. 2006. Recurring seasonal dynamics of microbial communities in stream habitats. Appl. Environ. Microbiol. 72:713-722. crossref(new window)

Islam, M.R., P.S. Chauhan, Y. Kim, M. Kim, and T.M. Sa. 2011. Community level functional diversity and enzyme activities in paddy soils under different long-term fertilizer management practices. Biol. Fert. Soils. DOI: 10.1007/s00374-010-0524-2.

Jin, M., Z.G. Zhao, Z.G. Qiu, J.F. Wang, Z.L. Chen, Z.Q. Shen, C. Li, X.W. Wang, Y. Dong, and J.W. Li. 2010. Rapid method to extract high-quality RNA from activated sludge. Huan Jing Ke Xue. 31:260-265

Johnson, D., P.J. Vandenkoornhuyse, J.R. Leake, L. Gilbert, R.E. Booth, J.P. Grime, J.P.W. Young, and D.J. Read. 2004. Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol. 161:503-515. crossref(new window)

Johnson, D.E. 1998. Applied multivariate methods for data analysts. Brooks/Cole, Pacific Grove, CA, USA.

Junier, P., T. Junier, and K. Witzel. 2008. TRiFLe, a Program for in silico terminal restriction fragment length polymorphism analysis with user-defines sequence sets. Appl. Environ. Microbiol. 74:6452-6456. crossref(new window)

Kanagawa, T. 2003. Bias and artifacts in multitemplate polymerase chain reactions (PCR). J. Biosci. Bioeng. 96:317-323. crossref(new window)

Kaplan, C.W. and C.L. Kitts. 2003. Variation between observed and true terminal restriction fragment length is dependent on true TRF length and purine content. J. Microbiol. Meth. 54:121-125. crossref(new window)

Katsivela, E., E.R.B. Moore, D. Maroukli, C. Strompl, D. Pieper, and N. Kalogerakis. 2005. Bacterial community dynamics during in-situ bioremediation of petroleum waste sludge in land farming sites. Biodegradation. 16:169-180 crossref(new window)

Kemnitz, D., K.J. Chin, P. Bodelier, and R Conrad. Community analysis of methanogenic archaea within a riparian flooding gradient. Environ. Microbiol. 6:449-461.

Kennedy, N., S. Edwards, and N. Clipson. 2005. Soil bacterial and fungal community structure across a range of unimproved and semi-improved upland grasslands. Microb. Ecol. 50:463-473. crossref(new window)

Kent, A.D., D.J. Smith, B.J. Benson, and E.W. Triplett. 2003. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl. Environ. Microbiol. 69:6768-6776. crossref(new window)

Knauth, S., T. Hurek, and D. Brar. 2005. Reinhold-Hurek B. Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ. Microbiol. 7:1725-1733. crossref(new window)

Kotsyurbenko, O.R., K.J. Chin, M.V. Glagolev, S. Stubner, M.V. Simankova, A.N. Nozhevnikova, and R. Conrad. 2004. Acetoclastic and hydrogenotrophic methane production and methanogenic populations in an acidic West-Siberian peat bog. Environ. Microbiol. 6:1159-1173. crossref(new window)

Kraigher, B., T. Kosjek, E. Heath, B. Kompare, and I. Mandic-Mulec. 2008. Influence of pharmaceutical residues on the structure of activated sludge bacterial communities in wastewater treatment bioreactors. Water Res. 42:4578-4588. crossref(new window)

Krupp, G. and H.J. Gross. 1979. Rapid RNA sequencing: nucleases from Staphylococcus aureus and Neurospora crassa discriminate between uridine and cytidine. Nucleic Acids Res. 6:3481-3489 crossref(new window)

Kurata, S., T. Kanagawa, Y. Magariyama, K. Takatsu, K. Yamada, T. Yokomaku, and Y. Kamagata. 2004. Reevaluation and reduction of a PCR bias caused by reannealing of templates. Appl. Environ. Microbiol. 70:7545-7549. crossref(new window)

Kvist, T., B.K. Ahring, and P. Westermann. 2007. Archaeal diversity in Icelandic hot springs. FEMS Microbiol. Ecol. 59:71-80. crossref(new window)

Ladapo, J.A. and M.A. Barlaz. 1997. Isolation and characterization of refuse methanogens. J.Appl. Microbiol. 82:751-758. crossref(new window)

Lane, D.J., B. Pace, G.J. Olsen, D.A. Stahl, M.L. Sogin, and N.R. Pace. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Nat. Acad. Sci. 82:6955-6959. crossref(new window)

LaPara, T.M., C.H. Nakatsu, L.M. Panteea, and J.E. Alleman. 2002. Stability of the bacterial communities supported by a seven-stage biological process treating pharmaceutical wastewater as revealed by PCR-DGGE. Water Res. 36:638-646. crossref(new window)

Lee, C., J. Kim, K. Hwang, V. O'Flaherty, and S. Hwang. 2009. Quantitative analysis of methanogenic community dynamics in three anaerobic batch digesters treating different wastewater. Water Res. 43:57-165.

Lee, D.H., Y.G. Zo, and S.J. Kim. 1996. Nonradioactive method to study genetic profiles of natural bacterial communities by PCR single strand conformation polymorphism. Appl. Environ. Microbiol. 62:3112-3120.

Leser, T.D., J.Z. Amenuvor, T.K. Jensen, R.H. Lindecrona, M. Boye, and K. Møller. 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl. Environ. Microbiol. 68:673-690. crossref(new window)

Leybo, A.I., A.I .Netrusov, and R. Conrad. 2006. Effect of hydrogen concentration on the community structure of hydrogenotrophic methanogens studied by T-RFLP analysis of 16S rRNA gene amplicons. Microbiol. 75:683-688. crossref(new window)

Li, F., M.A.J. Hullar, and J.W. Lampe. 2007. Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J. Microbiol. Methods. 68:303-311. crossref(new window)

Liu, W.T., T.L. Marsh, H. Cheng, and L.J. Forney. 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.

Lord, N.S., C.W. Kaplan, P. Shank, C.L. Kitts, and S.L. Elrod. 2002. Assessment of fungal diversity using terminal restriction fragment (TRF) pattern analysis: comparison of 18S and ITS ribosomal regions. FEMS Microbiol. Ecol. 42:327-337. crossref(new window)

Lu, Y., T. Lueders, M.W. Friedrich, and R. Conrad. 2005. Detecting active methanogenic populations on rice roots using stable isotope probing. Environ. Microbiol. 7:326-336. crossref(new window)

Lueders, T. and M.W. Friedrich. 2003. Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl. Environ. Microbiol. 69:320-326. crossref(new window)

Lukow, T., P.F. Dunfield, and W. Liesack. 2000. Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol. Ecol. 3:241-247.

Luna. G.M., A. Dell'Anno, C. Corinaldesi, M. Armeni, and R. Danovaro. 2009. Diversity and spatial distribution of metal-reducing bacterial assemblages in ground waters of different redox conditions. Int. Microbiol. 12:153-159.

Luz, A.P., V.H., Pellizari, L.G. Whyte, and C.W. Greer. 2004. A survey of indigenous microbial hydrocarbon degradation genes in soils from Antarctica and Brazil. Can. J. Microbiol 50:323-333. crossref(new window)

MacKay, R.M. and W.F. Doolittle. 1981. Nucleotide sequences of Acnathamoeba castellanii 5S and 5.8S ribosomal ribonucleic acids: phylogenetic and comparative structural analyses. Nucleic Acids Res. 9:3321-3334. crossref(new window)

Marsh, T.L., P. Saxman, J. Cole, and J. Tiedje. 2000. Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis. Appl. Environ. Microbiol. 66:3616-3620. crossref(new window)

McGarvey, J.A, W.G. Miller, R. Zhang, Y. Ma, and F. Mitloehner. 2007. Bacterial population dynamics in dairy waste during aerobic and anaerobic treatment and subsequent storage. Appl. Environ. Microbiol. 73:193-202. crossref(new window)

McGarvey, J.A., W.G. Miller, S. Sanchez, C.J. Silva, and L.C. Whitehand. 2005. Comparison of bacterial populations and chemical composition of dairy wastewater held in circulated and stagnant lagoons. J. Appl. Microbiol. 99:867-877. crossref(new window)