Chapter 34 : Bacterial Secondary Productivity

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Bacterial Secondary Productivity, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815882/9781555813796_Chap34-1.gif /docserver/preview/fulltext/10.1128/9781555815882/9781555813796_Chap34-2.gif


Planktonic heterotrophic bacteria (bacterioplankton) are now recognized to be a large and metabolically active group that contributes significantly to the biomass and to the flow of carbon in aquatic systems. Various methods available to determine bacterial biomass production (BBP), those that employ radiolabeled precursors to estimate the rate of synthesis of nucleic acids and proteins have become the most widely used and are the focus of this chapter. In this chapter, the rationale, advantages, and disadvantages of the most commonly used methods based on the incorporation of thymidine (TdR) and leucine (Leu) methods are discussed. In addition, methods to determine empirically a conversion factor from thymidine or leucine incorporation to cells produced is presented as well as several procedures designed to test various assumptions of these methods. Alternative methods to determine BBP that do not rely on the uptake of radiolabeled compounds are also discussed in the chapter. The BBP measurement methods presented in this chapter estimate the total BBP and do not provide information on the relationship between bacterial diversity and metabolism. The chapter concludes with a review of novel methods that combine measurements of BBP with microscopy and molecular techniques to determine the proportion of total bacteria that are active, and the contribution to total BBP of specific phylogenetic groups.

Citation: Chin-Leo G, Evans C. 2007. Bacterial Secondary Productivity, p 421-433. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch34
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Alldredge, A. L. 1993. Production of heterotrophic bacteria inhabiting marine snow, p. 531–536. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
2. Ammerman, J. W.,, J. A. Fuhrman,, Å. Hagström, and, F. Azam. 1984. Bacterioplankton growth in seawater. I. Growth kinetics and cellular characteristics in seawater cultures. Mar. Ecol. Prog. Ser. 18: 3139.
3. Amon, R. M. W.,, and R. Benner. 1996. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 4: 4151.
4. Azam, F.,, T. Fenchel,, J. G. Field,, J. S. Gray,, L. A. Meyer-Reil, and, T. F. Thingstad. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257263.
5. Bell, R. T. 1990. An explanation for the variability in the conversion factor deriving bacterial cell production from incorporation of [ 3H]-thymidine. Limnol. Oceanogr. 35: 910915.
6. Bell, R. T. 1993. Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine, p. 495–504. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
7. Bell, R. T.,, and B. Riemann. 1989. Adenine incorporation into DNA as a measure of bacterial production in freshwater. Limnol. Oceanogr. 34: 435444.
8. Benner, R.,, J. D. Pakulski,, M. McCarthy,, J. I. Hedges, and, P. G. Hatcher. 1992. Bulk chemical characterization of dissolved organic matter in the ocean. Science 255: 15611564.
9. Bern, L. 1985. Autoradiographic studies of (methyl- 3H)thymidine incorporation in a cyanobacterium ( Microcystis wesenbergii)-bacterium association and in selected algae and bacteria. Appl. Environ. Microbiol. 49: 232233.
10. Buesing, N.,, and M. O. Gessner. 2003. Incorporation of radiolabeled leucine into protein to estimate bacterial production in plant litter, sediment, epiphytic biofilms, and water samples. Microb. Ecol. 45: 291301.
11. Button, D. K.,, and B. R. Robertson. 1993. Use of high-resolution flow cytometry to determine the activity and distribution of aquatic bacteria, p. 163–173. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J.Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
12. Carman, K. R. 1993. Microautoradiographic detection of microbial activity, p. 397–404. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
13. Chin-Leo, G.,, and R. Benner. 1992. Enhanced bacterio-plankton production and respiration at intermediate salinities in the Mississippi River plume. Mar. Ecol. Prog. Ser. 87: 87103.
14. Chin-Leo, G.,, and D. L. Kirchman. 1988. Estimating bacterial production in marine waters from the simultaneous incorporation of thymidine and leucine. Appl. Environ. Microbiol. 54: 19341939.
15. Chin-Leo, G.,, and D. L. Kirchman. 1990. Unbalanced growth in natural assemblages of marine bacterioplankton. Mar. Ecol. Prog. Ser. 63: 18.
16. Cho, B. C.,, and F. Azam. 1988. Heterotrophic bacterio-plankton production measurement by the tritiated thymi-dine incorporation method. Arch. Hydrobiol. Beih. Ergebn. Limnol. 31: 153162.
17. Christian, R. R.,, R. B. Hanson, and, S. Y. Newell. 1982. Comparison of methods for measurement of bacterial growth rates in mixed batch cultures. Appl. Environ. Microbiol. 43: 11601165.
18. Cole, J. J.,, S. Findlay, and, M. L. Pace. 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar. Ecol. Prog. Ser. 43: 110.
19. Cole, J. J.,, and M. L. Pace. 1995. Why measure bacterial production? A reply to the comment by Jahnke and Craven. Limnol. Oceanogr. 40: 441444.
20. Cottrell, M. T.,, and D. L. Kirchman. 2000. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66: 16921697.
21. Cottrell, M. T.,, and D. L. Kirchman. 2003. Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol. Oceanogr. 48: 168178.
22. Cottrell, M. T.,, and D. L. Kirchman. 2004. Single-cell analysis of bacterial growth, cell size, and community structure in the Delaware Estuary. Aquat. Microb. Ecol. 34: 139149.
23. Coveney, M. F.,, and R. G. Wetzel. 1988. Experimental evaluation of conversion factors for the ( 3H)thymidine incorporation assay for bacterial secondary productivity. Appl. Environ. Microbiol. 54: 160168.
24. Craven, D. B.,, and D. M Karl. 1984. Microbial RNA and DNA synthesis in marine sediments. Mar. Biol. 83: 129.
25. del Giorgio, P. A.,, J. J. Cole, and, A. Cimbleris. 1997. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385: 148151.
26. del Giorgio, P. A.,, and J. J. Cole. 1998. Bacterial growth efficiency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29: 503541.
27. del Giorgio, P. A.,, and J. J. Cole. 2000. Bacterial energetics and growth efficiency, p. 289–325. In D. Kirchman (ed.), Microbial Ecology of the Oceans. Wiley-Liss, Inc., New York, N.Y.
28. Douglas, J. D.,, J. A. Novitsky, and, R. O. Fournier. 1987. Microautoradiography-based enumeration of bacteria with estimates of thymidine-specific growth and production rates. Mar. Ecol. Prog. Ser. 36: 9199.
29. Ducklow, H. W. 2000. Bacterial production and biomass in the oceans, p. 85–120. In D. Kirchman (ed.), Microbial Ecology of the Oceans. Wiley-Liss, Inc., New York, N.Y.
30. Ducklow, H. W.,, and C. A. Carlson. 1992. Oceanic bacterial production. Adv. Microb. Ecol. 12: 113181.
31. Ducklow, H. W.,, and S. M. Hill. 1985. Tritiated thymi-dine incorporation and the growth of heterotrophic bacteria in warm core rings. Limnol. Oceanogr. 30: 260272.
32. Ducklow, H. W.,, and D. L. Kirchman. 1983. Bacterial dynamics and distribution during a spring diatom bloom in the Hudson River Plume. J. Plankton Res. 5: 333355.
33. Ducklow, H. W.,, D. L. Kirchman, and, H. L. Quinby. 1992. Determination of bacterioplankton growth rates during the North Atlantic spring phytoplankton bloom. Microb. Ecol. 24: 125144.
34. Ellenbroek, F. M.,, and T. E. Cappenberg. 1991. DNA synthesis and tritiated thymidine incorporation by heterotrophic freshwater bacteria in continuous culture. Appl. Environ. Microbiol. 57: 16751682.
35. Evans, C. T.,, B. Van Mooy,, R. G. Keil,, C. Greengrove, and, G. Chin-Leo. 2004. Isolation of DNA from Actively Growing Heterotrophic Bacteria using 5-Bromo-2′- Deoxyuridine. American Society of Limnology and Oceanography/The Oceanography Society, Honolulu, Hawaii.
36. Fallon, R. D.,, and S. Y. Newell. 1986. Thymidine incorporation by the microbial community of standing-dead Spartina alterniflora. Appl. Environ. Microbiol. 52: 12061208.
37. Ferguson, R. L.,, E. N. Buckley, and, A. V. Palumbo. 1984. Response of marine bacterioplankton to differential filtration and confinement. Appl. Environ. Microbiol. 47: 4955.
38. Findlay, S. 1993. Thymidine incorporation into DNA as an estimate of sediment bacterial production, p. 505–508. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
39. Fischer, H.,, and M. Pusch. 1999. Use of the [ 14C]leucine incorporation technique to measure bacterial production in river sediments and the epiphyton. Appl. Environ. Microbiol. 65: 44114418.
40. Fuhrman, J. A.,, and F. Azam. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar. Biol. 66: 109120.
41. Gilmour, C. C.,, M. E. Leavitt, and, M. P. Shiaris. 1990. Evidence against incorporating of exogenous thymidine by sulfate-reducing bacteria. Limnol. Oceanogr. 35: 14011409.
42. Grossart, H.,, and H. Ploug. 2000. Bacterial production and growth efficiencies: direct measurements on riverine aggregates. Limnol. Oceanogr. 45: 436445.
43. Hagström, Å. 1984. Aquatic bacteria: measurements and significance of growth, p. 495–501. In M. J. Klug and, C. A. Reddy (ed.), Current Perspectives In Microbial Ecology. American Society for Microbiology, Washington, D.C.
44. Hagström, Å,, U. Larsson,, P. Hörstedt, and, S. Normark. 1979. Frequency of dividing cells, a new approach to the determination of bacterial growth rates in aquatic environments. Appl. Environ. Microbiol. 37: 805812.
45. Hamasaki, K.,, R. A. Long, and, F. Azam. 2004. Individual cell growth rates of marine bacteria, measured by bromodeoxyuridine incorporation. Aquat. Microb. Ecol. 35: 217227.
46. Hanson, R. B.,, and H. K. Lowery. 1983. Nucleic acid synthesis in oceanic microplankton from the Drake Passage, Antarctic; evaluation of steady state growth. Mar. Biol. 73: 7989.
47. Herndl, G. J.,, E. Kaltenböck, and, G. Müller-Niklas. 1993. Dialysis bag incubation as a nonradiolabeling technique to estimate bacterioplankton production, p. 553–556. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
48. Hietanen, S.,, L. Tuominen, and, J. Kuparinen. 1999. Benthic bacterial production in the northern Baltic Sea measured using a modified [14C]leucine incorporation method. Aquat. Microb. Ecol. 20: 1320.
49. Hietanen, S.,, J. Kuparinen,, R. J. Oja, and, L. Tuominen. 2001. Different filtration treatments and centrifugation in measuring bacterial production in brackish waters. Boreal Environ. Res. 6: 221229.
50. Hietanen, S.,, J. M. Lehtimaeki,, L. Tuominen,, K. Sivonen, and, J. Kuparinen. 2002. Nodularia spp. (Cyano-bacteria) incorporate leucine but not thymidine: importance for bacterial-production measurements. Aquat. Microb. Ecol. 28: 99104.
51. Hobbie, J. E. 1988. A comparison of the ecology of planktonic bacteria in fresh and salt water. Limnol. Oceanogr. 33: 750764.
52. Hobbie, J. E.,, R. J. Daley, and, S. Jasper. 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33: 12251228.
53. Hollibaugh, J. T. 1988. Limitations of the [ 3H]thymidine method for estimating bacterial productivity due to thymi-dine metabolism. Mar. Ecol. Prog. Ser. 43: 1930.
54. Hollibaugh, J. T. 1994. Relationships between thymidine metabolism, bacterioplankton community metabolic capabilities, and sources of organic matter. Microb. Ecol. 28: 117131.
55. Hoppe, H.-G.,, K. Gocke,, R. Koppe, and, C. Begler. 2002. Bacterial growth and primary production along a north-south transect of the Atlantic Ocean. Nature 416: 168171.
56. Ingraham, J. L.,, O. Maaloe, and, F. C. Neidhardt. 1983. Growth of the Bacterial Cell. Sinauer Associates, Sunder-land, Mass.
57. Jahnke, R. A.,, and D. B. Craven. 1995. Quantifying the role of heterotrophic bacteria in the carbon cycle: a need for respiration rate measurements. Limnol. Oceanogr. 40: 436441.
58. Johnstone, B.,, and R. P. Jones. 1989. A study of the lack of (methyl- 3H)thymidine uptake and incorporation by chemolitotrophic bacteria. Microb. Ecol. 18: 7377.
59. Jørgensen, N. O. G. 1992. Incorporation of [ 3H]leucine and [ 3H]valine into protein of freshwater bacteria: uptake kinetics and intracellular isotope dilution. Appl. Environ. Microbiol. 58: 36383646.
60. Kamjunke, N.,, and S. Jähnichen. 2000. Leucine incorporation by Mycrocystis aeruginosa. Limnol. Oceanogr. 45: 741743.
61. Karl, D. M. 1981. Simultaneous rates of ribonucleic acid and deoxyribonucleic acid syntheses for estimating growth and cell division of aquatic microbial communities. Appl. Environ. Microbiol. 42: 802810.
62. Karl, D. M. 1982. Selected nucleic acid precursors in studies of aquatic microbial ecology. Appl. Environ. Microbiol. 44: 891902.
63. Karl, D. M. 1993. Microbial RNA and DNA synthesis derived from the assimilation of [2, 3H]-adenine, p. 471–482. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
64. Karl, D. M. 1994. Accurate estimation of the microbial loop processes and rates. Microb. Ecol. 28: 147150.
65. Karl, D. M.,, and C. D. Winn. 1984. Adenine metabolism and nucleic acid synthesis: applications to microbiological oceanography, p. 197–216. In J. Hobbie and, P. Williams (ed.), Heterotrophic Activity in the Sea. Plenum Press, New York, N.Y.
66. Kemp, P. F.,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.). 1993. Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
67. Kirchman, D. L. 1993. Leucine incorporation as a measure of biomass production by heterotrophic bacteria, p. 509–512. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
68. Kirchman, D. L.,, and H. W. Ducklow. 1993. Estimating conversion factors for thymidine and leucine methods for measuring bacterial production, p. 513–517. In P. F. Kemp,, B. F. Sherr,, E. B. Sherr, and, J. J. Cole (ed.), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Fla.
69. Kirchman, D. L.,, and M. P. Hoch. 1988. Bacterial production in the Delaware Bay estuary estimated from thymidine and leucine incorporation rates. Mar. Ecol. Prog. Ser. 32: 169178.
70. Kirchman, D. L.,, E. K’nees, and, R. E. Hodson. 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl. Environ. Microbiol. 49: 599607.
71. Kirchman, D. L.,, S. Y. Newell, and, R. E. Hodson. 1989. Incorporation versus biosynthesis of leucine: implications for measuring rates of protein synthesis and biomass production by bacteria in marine systems. Mar. Ecol. Prog. Ser. 32: 4749.
72. Kirschner, A. K. T.,, and B. Velimirov. 1999. Benthic bacterial secondary production via simultaneous 3H-thymidine and 14C-leucine incorporation, and its implication for the carbon cycles of a shallow macrophyte-dominated backwater system. Limnol. Oceanogr. 44: 18711881.
73. Kirschner, A. K. T.,, and B. Velimirov. 1999. Leucine incorporation by 3H-leucine centrifugation method for determining bacterial protein synthesis in freshwater samples. Aquat. Microb. Ecol. 17: 201206.
74. Kirschner, A. K. T.,, P. Wihlidal, and, B. Velimirov. 2004. Variability and predictability of the empirical conversion factor for converting 3H-thymidine uptake into bacterial carbon production for a eutrophic lake. J. Plankton Res. 26: 15591566.
75. Lee, S.,, and J. A. Fuhrman. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 53: 12981303.
76. Lemee, R.,, E. Rochelle-Newall,, F. Van Wambeke,, M.-D. Pizay,, P. Rinaldi, and, J.-P. Gattuso. 2002. Seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea. Aquat. Microb. Ecol. 29: 227237.
77. Malstrom, R. T.,, M. T. Cottrell,, H. Elifantz, and, D. L. Kirchman. 2005. Biomass production and assimilation of dissolved organic matter by Sar11 bacteria in the northwest Atlantic Ocean. Appl. Environ. Microbiol. 71: 29792986.
78. McDonough, R. J.,, R. W. Sanders,, K. G. Porter, and, D. L. Kirchman. 1986. Depth distribution of bacterial production in a stratified lake with an anoxic hypolimnion. Appl. Environ. Microbiol. 52: 9921000.
79. Moriarty, D. J. W. 1986. Measurement of bacterial growth rates in aquatic systems from rates of nucleic acid synthesis. Adv. Microb. Ecol. 9: 243292.
80. Moriarty, D. J. W. 1988. Accurate conversion factors for calculating bacterial growth rates from thymidine incorporation into DNA: elusive or illusive? Arch. Hydrobiol. Beih. Ergebn. Limnol. 31: 211217.
81. Nagata, T.,, and Y. Watanabe. 1990. Carbon and nitrogen-to-volume ratios of bacterioplankton grown under different nutritional conditions. Appl. Environ. Microbiol. 56: 99109.
82. Newell, S. Y.,, R. D. Fallon, and, P. S. Tabor. 1986. Direct microscopy of natural assemblages, p. 1–48. In J. S. Poindexter and, E. R. Leadbetter (ed.), Bacteria in Nature, vol. 2. Plenum, New York, N.Y.
83. Nielsen, J. L.,, D. Christensen,, M. Kloppenborg, and, P. H. Nielsen. 2003. Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ. Microbiol. 5: 202211.
84. Ouverney, C. C.,, and J. A. Fuhrman. 1999. Combined microautoradiography-16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl. Environ. Microbiol. 65: 17461752.
85. Pace, M. L.,, P. Del Giorgio,, D. Fischer,, R. Condon, and, M. Heather. 2004. Estimates of bacterial production using the leucine incorporation method are influenced by differences in protein retention of microcentrifuge tubes. Limnol. Oceanogr. Methods 2: 5561.
86. Pedrós-Alió, C.,, and S. Y. Newell. 1989. Microautoradiographic study of thymidine uptake in brackish waters around Sapelo Island, Georgia, USA. Mar. Ecol. Prog. Ser. 55: 8394.
87. Pernthaler, A.,, J. Pernthaler,, M. Schattenhofer, and, R. Amann. 2002. Identification of DNA-synthesizing bacterial cells in coastal North Sea plankton. Appl. Environ. Microbiol. 68: 57285736.
88. Pomeroy, L. R. 1974. The ocean’s food web: a changing paradigm. BioScience 9: 499504.
89. Porter, K. G.,, and Y. S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25: 943948.
90. Proctor, L. M.,, and J. A. Fuhrman. 1990. Viral mortality of marine bacteria and cyanobacteria. Nature 343: 6062.
91. Riemann, B.,, and R. Bell. 1990. Advances in estimating bacterial biomass and growth in aquatic systems. Arch. Hydrobiol. 118: 385402.
92. Riemann, B.,, R. T. Bell, and, N. O. G. Jørgensen. 1990. Incorporation of thymidine, adenine and leucine into natural bacterial assemblages. Mar. Ecol. Prog. Ser. 65: 8794.
93. Robarts, R. D.,, and T. Zohary. 1993. Fact or fiction—bacterial growth rates and production rates as determined by [methyl- 3H]thymidine? Adv. Microb. Ecol. 13: 371425.
94. Rivkin, R. B.,, and L. Legendre. 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291: 23982400.
95. Servais, P. 1995. Measurement of the incorporation rates of four amino acids into proteins for estimating bacterial production. Microb. Ecol. 29: 115128.
96. Servais, P.,, and G. Billen. 1991. Bacterial production measured by 3H-thymidine and 3H-leucine incorporation in various aquatic ecosystems. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 7381.
97. Sherr, E. B.,, and B. F. Sherr. 1987. High rates of consumption of bacteria by pelagic ciliates. Nature 325: 710711.
98. Sherr, E. B.,, B. F. Sherr, and, C. T. Sigmon. 1999. Activity of marine bacteria under incubated and “in situ” conditions. Aquat. Microb. Ecol. 20: 213223.
99. Shiah, F.,, and H. W. Ducklow. 1997. Bacterioplankton growth responses to temperature and chlorophyll variations in estuaries measured by thymidine:leucine incorporation ratio. Aquat. Microb. Ecol. 13: 151159.
100. Simon, M.,, and F. Azam. 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51: 201213.
101. Smith, D. C.,, and F. Azam. 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using [ 3H]leucine. Mar. Microb. Food Webs 6: 107114.
102. Smith, E. M.,, and P. A. Del Giorgio. 2003. Low fractions of active bacteria in natural aquatic communities? Aquat. Microbiol. Ecol. 31: 203208.
103. Steward, G. F.,, and F. Azam. 1999. Bromodeoxyuridine as an alternative to 3H-thymidine for measuring bacterial productivity in aquatic samples. Aquat. Microb. Ecol. 19: 5766.
104. Suberkropp, K.,, and H. Weyers. 1996. Application of fungal and bacterial production methodologies to decomposing leaves in streams. Appl. Environ. Microbiol. 62: 16101615.
105. Tabor, P. S.,, and R. A. Neihof. 1982. Improved microautoradiographic methods to determine individual microorganisms active in substrate uptake in natural waters. Appl. Environ. Microbiol. 44: 945.
106. Taylor, G. T.,, and M. L. Pace. 1987. Validity of eukaryotic inhibitors for assessing production and grazing mortality of marine bacterioplankton. Appl. Environ. Microbiol. 53: 119128.
107. Thomaz, S. M.,, and R. G. Wetzel. 1995. [ 3H]Leucine incorporation methodology to estimate epiphytic bacterial biomass production. Microb. Ecol. 29: 6370.
108. Tibbles, B. J. 1996. Effects of temperature on the incorporation of leucine and thymidine by bacterioplankton and bacterial isolates. Aquat. Microb. Ecol. 11: 239250.
109. Tibbles, B. J.,, C. L. Davis,, J. M. Harris, and, M. I. Lucas. 1992. Estimates of bacterial productivity in marine sediments and water from a temperate saltmarsh lagoon. Microb. Ecol. 23: 195209.
110. Toolan, T. 2001. Coulometric carbon-based respiration rates and estimates of bacterioplankton growth efficiencies in Massachusetts Bay. Limnol. Oceanogr. 46: 12981308.
111. Torréton, J. P.,, and M. Bouvy. 1991. Estimating bacterial DNA synthesis from [ 3H]thymidine incorporation: discrepancies among macromolecular extraction procedures. Limnol. Oceanogr. 36: 299306.
112. Tuominen, L. 1995. Comparison of leucine uptake methods and a thymidine incorporation method for measuring bacterial activity in sediment. J. Microbiol. Methods 24: 125134.
113. Turley, C. M.,, and E. D. Stutt. 2000. Depth-related cell-specific bacterial leucine incorporation rates on particles and its biogeochemical significance in the Northwest Mediterranean. Limnol. Oceanogr. 45: 419425.
114. Urbach, E.,, K. L. Vergin, and, S. J. Giovannoni. 1999. Immunochemical detection and isolation of DNA from metabolically active bacteria. Appl. Environ. Microbiol. 65: 12071213.
115. van Looij, A.,, and B. Riemann. 1993. Measurement of bacterial production in coastal marine environments using leucine: applications of a kinetic approach to correct for isotope dilution. Mar. Ecol. Prog. Ser. 102: 97104.
116. Van Mooy, B. A. S.,, A. H. Devol, and, R. G. Keil. 2004. Quantifying 3H-thymidine incorporation rates by a phylogenetically defined group of marine planktonic bacteria ( Bacteriodetes phylum). Environ. Microbiol. 6: 10611069.
117. White, P. A.,, J. Kalff,, J. B. Rasmussen, and, J. M. Gasol. 1991. The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb. Ecol. 21: 99108.
118. Wicks, R. J.,, and R. D. Robarts. 1987. The extraction and purification of DNA labeled with [methyl- 3H]thymi-dine in aquatic bacterial population studies. J. Plankton Res. 9: 11591166.
119. Winding, A. 1992. 3H-thymidine incorporation to estimate growth rates of anaerobic bacterial strains. Appl. Environ. Microbiol. 58: 26602662.
120. Zweifel, U. L.,, and Å. Hagström. 1995. Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (ghosts). Appl. Environ. Microbiol. 61: 21802185.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error