Skip to main content
SpringerLink
Log in

Quantitative comparisons ofin situ microbial biodiversity by signature biomarker analysis

  • Published:
Journal of Industrial Microbiology

Abstract

Microscopic examinations have convinced microbial ecologists that the culturable microbes recovered from environmental samples represent a tiny proportion of the extant microbiota. Methods for recovery and enzymatic amplification of nucleic acids from environmental samples have shown that a huge diversity existsin situ, far exceeding any expectations which were based on direct microscopy. It is now theoretically possible to extract, amplify and sequence all the nucleic acids from a community and thereby gain a comprehensive measure of the diversity as well as some insights into the phylogeny of the various elements within this community. Unfortunately, this analysis becomes economically prohibitive if applied to the multitude of niches in a single biome let alone to a diverse set of environments. It is also difficult to utilize PCR amplification on nucleic acids from some biomes because of coextracting enzymatic inhibitors. Signature biomarker analysis which potentially combines gene probe and lipid analysis on the same sample, can serve as a complement to massive environmental genome analysis in providing quantitative comparisons between microniches in the biome under study. This analysis can also give indications of the magnitude of differences in biodiversity in the blome as well as provide insight into the phenotypic activities of each community in a rapid and cost-effective manner. Applications of signature lipid biomarker analysis to define quantitatively the microbial viable biomass of portions of an Eastern USA deciduous forest, are presented.

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

Similar content being viewed by others

References

  1. Almeida JS, A Sonesson, DB Ringelberg and DC White. 1995. Application of artificial neural networks (ANN) to the detection ofMycobacterium tuberculosis, its antibiotic resistance and prediction of pathogenicity amongstMycobacterium spp based on signature lipid biomarkers. Binary—Computing in Microbiology 7: 53–59.

    Google Scholar 

  2. Anderson TA, DC White and BT Walton. 1995. Degradation of hazardous organic compounds by rhizosphere microbial communities. In: Biotransformations: Microbial Degradation of Health-Risk Compounds (VP Singh, ed), pp 205–225, Elsevier, The Netherlands.

    Google Scholar 

  3. Balkwill DL, FR Leach, JT Wilson, JF McNabb and DC White. 1988. Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosine triphosphate, and direct counts in subsurface sediments. Microbial Ecol 16: 73–84.

    Google Scholar 

  4. Balkwill DL. 1989. Numbers, diversity and morphological characteristics of aerobic, chemoheterotrophic bacteria from the deep subsurface. Geomicrobiol J 7: 33–52.

    Google Scholar 

  5. Bhat RU and RW Carlson. 1992. A new method for the analysis of amide-linked hydroxy fatty acids in lipid-A from Gram-negative bacteria. Glycobiology 2: 535–539.

    PubMed  Google Scholar 

  6. Bobbie RJ, JS Nickels, GA Smith, SD Fazio, RH Findlay, WM Davis and DC White. 1981. Effect of light on biomass and community structure of estuarine detrital microbiota. Appl Environ Microbiol 42: 150–158.

    Google Scholar 

  7. Boone TL and DL Balkwill. 1988. Morphological and cultural comparison of microorganisms in subsurface soil and subsurface sediments at a pristine study site in Oklahoma. Microbial Ecol 16: 85–97.

    Google Scholar 

  8. Bratbak G and I Dundas. 1984. Bacterial dry matter content and biomass estimations. Appl Environ Microbiol 48: 755–757.

    PubMed  Google Scholar 

  9. Brennan PJ. 1988. Mycobacterium and other actinomycetes. In: Microbial Lipids, vol 1 (Ratledge C and SG Wilkinson, eds), p 217, Academic Press, London.

    Google Scholar 

  10. Brinch-Iverson J and GM King. 1990. Effects of substrate concentration, growth state, and oxygen availability on relationships among bacterial carbon, nitrogen and phospholipid phosphorous content. FEMS Microbial Ecol 74: 345–356.

    Google Scholar 

  11. Canuel EA, JE Cloen, DB Ringelberg, JB Guckert and GH Rau. 1995. Molecular and isotopic tracers used to examine sources of organic matter and its incorporation into the food webs of San Francisco Bay. Limnol Oceanogr 40: 67–81.

    Google Scholar 

  12. Coleman ML, DB Hedrick, DR Lovely, DC White and K Pye. 1993. Reduction of Fe(III) in sediments by sulfate-reducing bacteria. Nature 361: 436–438.

    Google Scholar 

  13. Collins MD, RM Keddie and RM Kroppenstedt. 1983. Lipid composition ofArthrobacter simplex, Arthrobacter tumescens, and possibly related taxa. Syst Appl Microbiol 4: 18–26.

    Google Scholar 

  14. Dickinson CH. 1986. Adaptations of micro-organisms to climatic conditions affecting aerial plant surfaces. In: Microbiology of the Phyllosphere (Fokkema NJ and J VandenHeuvel, eds), pp 77–100, Cambridge Univ Press, New York.

    Google Scholar 

  15. Doi Y. 1990. Microbial Polyesters. pp 1–8. VCH Publishers, New York.

    Google Scholar 

  16. Dowling NJE, F Widdel and DC White. 1986. Phospholipid esterlined fatty acid biomarkers of acetate-oxidizing sulfate reducers and other sulfide forming bacteria. J Gen Microbiol 132: 1815–1825.

    Google Scholar 

  17. Edlund A, PD Nichols, R Roffey and DC White. 1985. Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles fromDesulfovibrio species. J Lipid Res 26: 982–988.

    PubMed  Google Scholar 

  18. Federle TW, MA Hullar, RJ Livingston, DA Meeter and DC White. 1983. Spatial distribution of biochemical parameters indicating biomass and community composition of microbial assemblies in estuarine mud flat sediments. Appl Environ Microbiol 45: 58–63.

    Google Scholar 

  19. Findlay RH and DC White. 1983. Polymeric beta-hydroxyalkanoates from environmental samples andBacillus megaterium. Appl Environ Microbiol 45: 71–78.

    Google Scholar 

  20. Findlay RH and DC White. 1983. The effects of feeding by the sand dollarMellita quinquiesperforata on the benthic microbial community. J Exp Mar Biol Ecol 72: 25–41.

    Google Scholar 

  21. Findlay RH, GM King and L Watling. 1989. Efficiency of phospholipid analysis in determining microbial biomass in sediments. Appl Environ Microbiol 55: 2888–2895.

    Google Scholar 

  22. Findlay RH, MB Trexler, JB Guckert and DC White. 1990. Laboratory study of disturbance in marine sediments: response of a microbial community. Mar Ecol Prog Ser 61: 121–133.

    Google Scholar 

  23. Findlay RH, MB Trexler and DC White. 1990. Response of a benthic microbial community to biotic disturbance. Mar Ecol Prog Ser 61: 135–148.

    Google Scholar 

  24. Findlay RH and FC Dobbs 1993. Quantitative description of microbial communities using lipid analysis. In: Handbook of Methods in Aquatic Microbial Ecology (Kemp PF, BF Sherr, EB Sherr and JJ Cole, eds), pp 271–284, Lewis Publishers, Boca Raton, RL.

    Google Scholar 

  25. Fredrickson JK, DL Baldwill, GR Drake, MF Romine, DB Ringelberg and DC White. 1995. Aromatic-degradingSphingomonas isolates from the deep subsurface. Appl Environ Microbiol 61: 1917–1922.

    PubMed  Google Scholar 

  26. Fredrickson JK, JP McKinley, SA Nierzwicki-Bauer, DC White, DB Ringelberg, SA Rawson, S-M Li, FJ Brockman and BN Bjornstad. 1995. Microbial community structure and biogeochemistry of miocene subsurface sediments: implications for long-term microbial survival. Molec Ecol 4: 619–626.

    Google Scholar 

  27. Frostegaard A, A Tunlid and E Baath. 1991. Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14: 151–163.

    Google Scholar 

  28. Gehron MJ and DC White. 1982. Quantitative determination of the nutritional status of detrital microbiota and the grazing fauna by triglyceride glycerol analysis. J Exp Mar Biol 64: 145–158.

    Google Scholar 

  29. Guckert JB, CP Antworth, PD Nichols and DC White. 1985. Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31: 147–158.

    Google Scholar 

  30. Guckert JB, MA Hood and DC White. 1986. Phospholipid, esterlinked fatty acid profile changes during nutrient deprivation ofVibriocholerae: increases in thetrans/cis ratio and proportions of cyclopropyl fatty acids. Appl Environ Microbiol 52: 794–801.

    PubMed  Google Scholar 

  31. Guckert JB, DB Ringelberg, DC White, RS Henson and BJ Bratina. 1991. Membrane fatty acids as phenotypic markers in the polyphasic taxonomy of methylotrophs within the proteobacteria. J Gen Microbiol 137: 2631–2641.

    PubMed  Google Scholar 

  32. Haldeman DL and PS Amy. 1993. Bacterial heterogeneity in deep subsurface tunnels at Rainer Mesa, Nevada test site. Microbiol Ecol 25: 183–194.

    Google Scholar 

  33. Haldeman DL, PS Amy, DB Ringelberg and DC White. 1993. Characterization of the microbiology within a 21 M3 section of rock from the deep subsurface. Microbiol Ecol 26: 145–159.

    Google Scholar 

  34. Hedrick DB and DC White. 1986. Microbial respiratory quinones in the environment: a sensitive liquid chromatographic method. J Microbiol Meth 5: 243–254.

    Google Scholar 

  35. Hedrick DB, JB Guckert and DC White. 1991. The effect of oxygen and chloroform on microbial activities in a high-solids, high-productivity biomass reactor. Biomass & Bioenergy 1: 207–212.

    Google Scholar 

  36. Hedrick DB, A Vass, B Richards, W Jewell, JB Guckert and DC White. 1991. Starvation and overfeeding stress on microbial activities in high-solids high-yield methanogenic high yield digesters. Biomass & Bioenergy 1: 75–82.

    Google Scholar 

  37. Hedrick DB, JB Guckert and DC White. 1991. Archaebacterial ether lipid diversity analyzed by supercritical fluid chromatography: integration with a bacterial lipid protocol. J Lipid Res 32: 659–666.

    PubMed  Google Scholar 

  38. Hedrick DB, RD Pledger, DC White and JA Baross. 1992.In situ microbial ecology of hydrothermal vent sediments. FEMS Microbiol Ecol 101: 1–10.

    Google Scholar 

  39. Heipieper H-J, R Diffenbach and H Keweloh. 1992. Conversion ofcis unsaturated fatty acids totrans, a possible mechanism for the protection of phenol degradingPseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58: 1847–1852.

    PubMed  Google Scholar 

  40. Intriago P. 1992. The regulation of fatty acid biosynthesis in some estuarine strains ofFlexibacter. J Gen Microbiol 138: 109–114.

    Google Scholar 

  41. Kaufman MG, MJ Klug and RW Merritt. 1989. Growth and food utilization parameters of germ-free house crickets,Acheta domesticus. J Insect Physiol 35: 957–967.

    Google Scholar 

  42. Kehrmeyer SR, BM Appelgate, HC Pinkart, DB Hedrick, DC White and GS Sayler. 1996. Combined lipid/DNA extraction method for environmental samples. J Microbiol Meth 25: 153–163.

    Google Scholar 

  43. Keift TL, DB Ringelberg and DC White. 1994. Changes in ester-linked phospholipid fatty acid profiles of subsurface bacteria during starvation and dessication in a porus medium. Appl Environ Microbiol 119: 303–308.

    Google Scholar 

  44. Kerger DB, PD Nichols, W Sand, E Bock and DC White. 1987. Association of acid-producingThiobacilli with degradation of concrete: analysis by ‘signature’ fatty acids from the polar lipids and lipopolysaccharide. J Ind Microbiol 2: 63–69.

    Google Scholar 

  45. Kerger DB, CA Mancuso, PD Nichols, DC White, T Langworthy, M Sittig, H Schlessner and P Hirsch. 1988. The budding bacteria,Pirellula andPlanctomyces, with a typical 16S-rRNA and absence of peptidoglycan, show eubacterial phospholipids and unusually high proportions of long-chain beta-hydroxy fatty acids in the lipopolysaccharide lipid A. Arch Microbiol 149: 255–260.

    Google Scholar 

  46. Kim H-Y, T-C Wang and Y-C Ma. 1994. Liquid chromatography/mass spectrometry of phospholipids using electrospray ionization. Ann Chem 66: 3977–3982.

    Google Scholar 

  47. Kohring LL, DB Ringelberg, R Devereux, D Stahl, MW Mittelman and DC White. 1994. Comparison of phylogenetic relationships based on phospholipid fatty acid profiles and ribosomal RNA sequence similarities among dissimilatory sulfate-reducing bacteria. FEMS Microbiol Lett 119: 303–308.

    PubMed  Google Scholar 

  48. Lennarz WJ. 1970. Bacterial lipids. In: Lipid Metabolism (Wakil S, ed), pp 155–183, Academic Press, New York, NY.

    Google Scholar 

  49. Lovely DR, SJ Giovannoni, DC White, JE Champine, EJP Phillips, YA Gorby and S Goodwin. 1992.Geobacter metallireducens gen nov sp nov, a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159: 363–344.

    Google Scholar 

  50. Maybery WM and JR Lane. 1993. Sequential alkaline saponification/acidhydrolysis/esterification: a one-tube method with enhanced recovery of both cyclopropane and hydroxylated fatty acids. J Microbial Meth 18: 21–32.

    Google Scholar 

  51. Mikell AT Jr, TJ Phelps and DC White. 1987. Phospholipids to monitor microbial ecology in anaerobic digesters. In: Methane from Biomass, a Systems Approach (Smith WH and JR Frank, eds), pp 413–444, Elsevier Pub Co, New York, NY.

    Google Scholar 

  52. Minnikin DE and H Abdolrahimzadeh. 1974. The replacement of phosphatidylethanlolamine and acidic phospholipids by ornithine-amide lipid and a minor phosphorus-free lipid inPseudomonas fluorescens NCMB 129. FEBS Lett 43: 257–260.

    PubMed  Google Scholar 

  53. Montagna PA. 1982. Sampling design and enumeration statistics for bacteria extracted from marine sediments. Appl Environ Microbiol 43: 1366–1372.

    Google Scholar 

  54. morrison SJ, JD King, RJ Bobbie, RE Bechtold and DC White. 1977. Evidence for microfloral succession on allochthonous plant litter in Apalachicola Bay, Florida, USA. Mar Biol 41: 229–240.

    Google Scholar 

  55. Morrison SJ and DC White. 1980. Effects of grazing by estuarine gammaridean amphipods on the microbiota of allochthonous detritus. Appl Environ Microbiol 40: 659–671.

    Google Scholar 

  56. Nes WR. 1977. The biochemistry of plant sterols. Adv Lip Res 15: 233–324.

    Google Scholar 

  57. Newell SY. 1993. Membrane-containing fungal mass and fungal specific growth rate in natural samples. In: Handbook of Methods in Aquatic Microbial Ecology (Kemp PF, BF Sherr, EB Sherr and JJ Cole, eds), pp 579–586, Lewis Publishers, Boca Raton, FL.

    Google Scholar 

  58. Nichols PD, WR Mayberry, CP Antworth and DC White. 1985. Determination of monounsaturated double bond position and geometry in the cellular fatty acids of the pathogenic bacteriumFrancisella tularensis. J Clin Microbiol 21: 738–740.

    PubMed  Google Scholar 

  59. Nichols PD, GA Smith, CP Antworth, RS Hanson and DC White. 1985. Phospholipid and lipopolysaccharide normal and hydroxy fatty acids as potential signatures for the methane-oxidizing bacteria. FEMS Microbial Ecol 31: 327–335.

    Google Scholar 

  60. Nichols PD, BK Stulp, JG Jones and DC White. 1986. Comparison of fatty acid content and DNA homology of the filamentous gliding bacteriaVitreoscilla, Flexibacter, Filibacter. Arch Microbiol 146: 1–6.

    Google Scholar 

  61. Nichols PD, CA Mancuso and DC White. 1987. Measurement of methanotroph and methanogen signature phospholipids for use in assessment of biomass and community structure in model systems. Org Geochem 11: 451–461.

    Google Scholar 

  62. Nickels JS, JD King and DC White. 1979. Poly-beta-hydroxybutyrate accumulation as a measure of unbalanced growth of the estuarine detrital microbiota. Appl Environ Microbiol 37: 459–465.

    Google Scholar 

  63. Odham G, A Tunlid, G Westerdahl, L Larsson, JB Guckert and DC White. 1985. Determination of microbial fatty acid profiles as femtomolar levels in human urine and the initial marine microfouling community by capillary gas chromatography-chemical ionization mass spectrometry with negative ion detection. J Microbiol Meth 3: 331–344.

    Google Scholar 

  64. Ogram A, GS Sayler and T Barkay. 1987. The extraction and purification of microbial DNA from sediments. J Microbiol Meth 7: 57–66.

    Google Scholar 

  65. Olsson PA, E Bååth, I Jacobson and B Söderströrom. 1995. The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99: 623–629.

    Google Scholar 

  66. O'Neill EG and RG Norby. 1996. Litter quality and decomposition rates of foliar litter produced under CO2 enirchment. In: Carbon Dioxide and Terrestrial Ecosystems (Koch GW and HA Moody, eds), pp 67–103, Academic Press, San Diego.

    Google Scholar 

  67. Parker JH, GA Smith, HL Fredrickson, JR Vestal and DC White. 1982. Sensitive assay, based on hydroxy-fatty acids from lipopolysaccharide lipid A for Gram negative bacteria in sediments. Appl Environ Microbiol 44: 1170–1177.

    PubMed  Google Scholar 

  68. Parkes RJ, NJE Dowling, DC White, RA Herbert and GR Gibson. 1992. Characterization of sulfate-reducing bacterial populations within marine and estuarine sediments with different rates of sulfate reduction. FEMS Microbial Ecol 102: 235–250.

    Google Scholar 

  69. Phelps TJ, SM Pfiffner, KA Sargent and DC White. 1994. Factors influencing the abundance and metabolic capacities of microorganisms in eastern coastal plain sediments. Microbiol Ecol 28: 351–364.

    Google Scholar 

  70. Pinkart HC, JW Wolfram, R Rogers and DC White. 1996. Cell envelope changes in solvent-tolerant and solvent-sensitivePseudomonas putida strains following exposure toO-xylene. Appl Env Microbiol 62: 1127–1131.

    Google Scholar 

  71. Rezenka T, IV Zlatkin, I, Viden, OI Slabova and DI Nikitin. 1991. Capillary gas chromatography-mass spectrometry of unusual and very long-chain fatty acids from soil oligotrophic bacteria. J Chrom 558: 215–221.

    Google Scholar 

  72. Ringelberg DB, JD Davis, GA Smith, SM Pfiffner, PD Nichols, JB Nickels, JM Hensen, JT Wilson, M Yates, DH Kampbell, HW Reed, TT Stocksdale and DC White. 1988. Validation of signature polarlipid fatty acid biomarkers for alkane-utilizing bacteria in soils and subsurface aquifer materials. FEMS Microbial Ecol 62: 39–50.

    Google Scholar 

  73. Ringelberg DB, T Townsend, KA DeWeerd, JM Suflita and DC White. 1994. Detection of the anaerobic declorinatorDesulfomonile tiedjei in soil by its signature lipopolysaccharide branched-long-chain hydroxy fatty acids. FEMS Microbiol Ecol 14: 9–18.

    Google Scholar 

  74. Ringelberg DB, JO Stair, J Almeida, RJ Norby, EG O'Neill and DC White. 1996. Consequences from rising atmospheric CO2 levels on the below-ground microbiota associated withQuercus alba L. Environ Qual (in press).

  75. Seckbach J, R Ikan, DB Ringelberg and DC White. 1993. Sterols and phylogeny of the acidophilic hot springs algaeCyanidium caldarium andGaldieria sulphurara. Phytochemistry 34: 1345–1349.

    Google Scholar 

  76. Sikkema J, JAM deBont and B Poolman. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201–222.

    PubMed  Google Scholar 

  77. Smith GA, PD Nichols and DC White. 1989. Triglyceride and sterol and composition of sediment microorganisms from McMurdo Sound, Antarctica. Polar Biol 9: 273–279.

    Google Scholar 

  78. Smith GA, JS Nickels, BD Kerger, JD Davis, SP Collins, JT Wilson, JF McKnabb and DC White. 1986. Quantitative characterization of microbial biomass and community structure in subsurface material: a prokaryotic consortium responsive to organic contamination. Can J Microbiol 32: 104–111.

    Google Scholar 

  79. Tunlid A, BH Baird, MB Trexler, S Olsson, RH Findlay, G Odham and DC White. 1985. Determination of phospholipid ester-linked fatty acids and poly beta hydroxybutyrate for the estimation of bacterial biomass and activity in the rhizosphere of the rape plantBrassica napus (L). Can J Microbiol 31: 1113–1119.

    Google Scholar 

  80. Tunlid A and DC White. 1991. Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of the microbial communities in soil. In: Soil Biochemistry (Bollag J-M and G Stotzky, eds), Vol 7, pp 229–262, Marcel Dekker, New York, NY.

    Google Scholar 

  81. Walker JT, A Sonesson, CW Keevil and DC White. 1993. Detection ofLegionella pneumophila in biofilms containing a complex microbial consortium by gas chromatography-mass spectrometric analysis of genus-specific hydroxy fatty acids. FEMS Microbiol Lett 113: 139–144.

    PubMed  Google Scholar 

  82. Walker RW. 1969. Cis-11-hexadecenoic acid fromCytophaga hutchinsonii lipids. Lipids 4: 15–18.

    PubMed  Google Scholar 

  83. White DC, WM Davis, JS Nickels, JD King and RJ Bobbie. 1979. Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40: 51–62.

    Google Scholar 

  84. White DC, RJ Bobbie, JS Nickels, SD Fazio and WM Davis. 1980. Nonselective biochemical methods for the determination of fungal mass and community structure in estuarine detrital microflora. Botanica Marina 23: 239–250.

    Google Scholar 

  85. White DC. 1983. Analysis of microorganisms in terms of quantity and activity in natural environments. In: Microbes in their Natural Environments (Slater JH, R Whittenbury and JWT Wimpenny, eds), pp 37–66, Society for General Microbiology Symposium.

  86. White DC, GA Smith and GR Stanton. 1984. Biomass, community structure, and metabolic activity of the microbiota in benthic marine sediments and sponge spicule mats. Antarctic J US 29: 125–126.

    Google Scholar 

  87. White DC. 1986. Environmental effects testing with quantitative microbial analysis: chemical signatures correlated within situ biofilm analysis by FT/IR. Tox Assess 1: 315–338.

    Google Scholar 

  88. White DC. 1988. Validation of quantitative analysis for microbial biomass, community structure, and metabolic activity. Adv Limnol 31: 1–18.

    Google Scholar 

  89. White DC, DB Ringelberg, JB Guckert and TJ Phelps. 1991. Biochemical markers for measuringin situ microbial community structure. In: Proceedings of the First International Symposium on Microbiology of the Deep Subsurface (Fliermans CB and TC Hazen, eds), pp 4.45–4.56, Jan 15–21, 1990, Orlando, FL. WSRC Information Services, Aiken, SC.

    Google Scholar 

  90. White DC. 1994. Is there anything else you need to understand about the microbiota that cannot be derived from analysis of nucleic acids? Microb Ecol 28: 163–166.

    Google Scholar 

  91. White DC. 1995. Chemical ecology: possible linkage between macro-and microbial ecology. Oikos 74: 174–181.

    Google Scholar 

  92. White DC, HC Pinkart and DB Ringelberg. 1995. Biomass measurements: biochemical approaches. In: Manual of Environmental Microbiology, 1st edn (Hurst CH, G Knudsen, M McInerney, LD Stetzenbach and M Walter, eds), pp 91–101, American Society for Microbiology Press, Washington, DC.

    Google Scholar 

  93. White DC and DB Ringelberg. 1996. Monitoring deep subsurface microbiota for assessment of safe long term nuclear waste disposal. Can J Microbiol 42: 375–381.

    Google Scholar 

  94. White DC and DB Ringelberg. 1996. Utility of signature lipid biomarker analysis in determiningin situ viable biomass, community structure, and nutritional/physiological status of the deep subsurface microbiota. In: The Microbiology of the Terrestrial Subsurface (Amy PS and DL Haldeman. eds), CRC Press, Boca Raton, FL.

    Google Scholar 

  95. White DC and SJ MacNaughton. 1996. Chemical and molecular approaches for rapid assessment of the biological status of soils. In: Bioindicators of Soil Health (Parkhurst CE, BM Doube and VVSR Gupa, eds), CAB International, Wallingford, UK.

    Google Scholar 

  96. White DC, DB Ringelberg and RJ Palmer. 1996. Quantitative comparison of thein situ microbial communities in different biomes. Seventh International Symposium on Microbial Ecology, Santos, Brazil.

  97. Zac DR, DB Ringelberg, KS Pregitzer, DL Randlett, DC White and PS Curtis. 1996. Soil microbial communities beneathPopulus grandidentata grown under elevated atmospheric CO2. J Ecol Appl 6: 257–262.

    Google Scholar 

  98. Zogg GP, DR Zak, DB Ringelberg, NW MacDonald, KS Pregitzer and DC White. 1996. Compositional and functional shifts in microbial communities related to soil warming. Soil Sci Soc Am J (in press).

Download references

Author information

Authors and Affiliations

  1. Center for Environmental Biotechnology, University of Tennessee, 10515 Research Drive, Suite 300, 37932-2575, Knoxville, TN, USA

    DC White, JO Stair & DB Ringelberg

  2. Environmental Sciences Division, Oak Ridge National Laboratory, 37983, Oak Ridge, TN, USA

    DC White

  3. Department of Microbiology, University of Tennessee, 37932-2575, Knoxville, TN, USA

    DC White

Authors
  1. DC White
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. JO Stair
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. DB Ringelberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, D., Stair, J. & Ringelberg, D. Quantitative comparisons ofin situ microbial biodiversity by signature biomarker analysis. Journal of Industrial Microbiology & Biotechnology 17, 185–196 (1996). https://doi.org/10.1007/BF01574692

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01574692

Keywords

Search

Navigation