Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem

Applied and Environmental Microbiology

Volumn 71, Issue 12, 2005, Pages 7737-7749

  Longnecker, K ^a,b   Sherr, B F ^a   Sherr, E B ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ELECTRON TRANSITIONS; ELECTROPHORESIS; METABOLISM; MICROBIOLOGY; NUCLEIC ACIDS;

BACTERIPLANKTON METABOLIC ACTIVITY; NUCLEIC ACID CONTENT (HNA); PHYLOGENETIC DIVERSITY; SHELF WATERS;

CELLS;

DNA; SEA WATER;

BACTERIUM; METABOLISM; PHYLOGENETICS; UPWELLING;

ACTINOBACILLUS; ARTICLE; BACTERIAL CELL; BACTEROIDES; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; ECOSYSTEM; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC VARIABILITY; NONHUMAN; OCEANIC REGIONS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEOBACTERIA; WATER SAMPLING;

BACTERIA; CHLOROPHYLL; ECOSYSTEM; ELECTRON TRANSPORT; LEUCINE; NITRATES; NUCLEIC ACIDS; PHYLOGENY; SEAWATER; TEMPERATURE;

ACTINOBACILLUS; BACTERIA (MICROORGANISMS); BACTEROIDES; PROTEOBACTERIA;

EID: 29144498686     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.12.7737-7749.2005     Document Type: Article

References (77)

1. Bano, N., and J. T. Hollibaugh. 2002. Phylogenetic composition of baeterio-plankton assemblages from the Arctic Ocean. Appl. Environ. Microbiol. 68:505-518.
2. Bernard, L., C. Courties, C. Duperray, II. Schäfer, G. Muyzer, and P. Leharon. 2001. A new approach to determine the genetic diversity of viable and active bacteria in aquatic ecosystems. Cytometry 43:314-321.
3. Bernard, L., C. Courties, P. Servais, M. Troussellier, M. Petit, and P. Lebaron. 2000. Relationships among bacterial cell size, productivity, and genetic diversity in aquatic environments using cell sorting and flow cytometry. Microb. Ecol. 40:148-158.
4. Bernard, L., H. Schäfer, K. Joux, C. Courties, G. Muyzer, and P. Lebaron. 2000. Genetic diversity of total, active and culturable marine bacteria in coastal seawater. Aquat. Microb. Ecol. 23:1-11.
5. Britschgi, T. B., and S. J. Giovannoni. 1990. Phylogenctic analysis of a natural marine baetcrioplankton population by rRNA gene cloning and sequencing. Appl. Environ. Microbiol. 57:1707-1713.
6. Button, D. K., and B. R. Robertson. 2001. Determination of DNA content of aquatic bacteria by flow cytometry. Appl. Environ. Microbiol. 67:1636-1717.
7. Casotti, R., C. Brunet, B. Aronne, and M. Ribera d'Aleala, 2000. Mesoscale features of phytoplankton and planktonic bacteria in a coastal area as induced by external water masses. Mar. Ecol. Prog. Scr. 195:15-27.
8. Chavez, F. P., J. T. Pennington, C. G. Castro, J, P. Ryan, R. P. Miehisaki, B. Schlining, P. Walz, K. R. Buck, A. McFadyen, and C. A. Collins. 2002. Biological and chemical consequences of the 1997-1998 El Niño in central California waters. Prog. Oceanogr. 54:205-232.
9. Cottrell, M. T., and D, L. Kirehman, 2003. Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol. Oceanogr. 48:168-178.
10. Cottrell, M. T., and L. L. Kirchman. 2000. Natural assemblages of marine proteobacteria and members of the Cytophaga cluster consuming low- and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66: 1692-1697.
11. 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. 34:139-149.
12. del Giorgio, P. A., and T. C. Bouvier. 2002. Linking the physiologic und phylogenetic successions in free-living bacterial communities along an estnarine salinity gradient. Limnol. Oceanogr. 47:471-486.
13. del Giorgio, P. A., Y. T. Prairie, and D. F. Bird. 1997. Coupling between rates of bacterial production and the iuiniher of nictabolically active cells in lake hacterioplankton, measured using CTC reduction and flow cytometry. Microb. Ecol. 34:144-154.
14. DeLong, K. F., D. G. Franks, A. L. Alldredge. 1993. Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol. Oceanogr. 38:924-934.
15. Dietz, E. J. 1983. Permutation tests for association between two distance matrices. Syst. Ecol. 32:21-26.
16. Ducklow, H.W. 1999. The bacterial component of the oceanic cuphotic zone. FEMS Microbiol. Ecol. 30:1-10.
17. Eilers, H., J. Pernthaler, F. O. Glöckner, and R. Amann. 2000. Culturability and in situ abundance of pelngic bacteria from the North Sea. Appl. Environ. Microbiol. 66:3044-3051.
18. Ferrari, B. C., G. Oregaard, and S. J. Sørensen. 2004. Recovery of GFP-labeled bacteria for culturing and molecular analysis alter cell sorting using a benchlop flow cytometer. Microb. Ecol. 48:239-245.
19. Fuchs, B. M., M. V. Zubkov, K. Sahm, P. H. Burkill, and R. Amann. 2000. Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques. Environ. Microbiol. 2:191-201.
20. Fuhrman, J. A., and A. A. Davis, 1997. Widespread Archaca and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150:275-285.
21. Fuhrman, J. A., K. McCallum, and A. A. Davis, 1993. Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific oceans. Appl. Environ. Microbiol. 59:1294-1302.
22. Gasol, J. M., and P. A. del Giorgio. 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 64:197-224.
23. Gasol, J. M., U. L. Zweifel, F. Peters, J. A. Fuhrman, and Å. Hagström. 1999. Significance of size and nucleic acid content in heterogeneity as measured by How cytometry in natural planktonic bacteria. Appl. Environ. Microbiol. 65:4475-4483.
24. Giovunnoni, S. J., T. B. Britsehgi, C. L. Moyer, and K. G. Field. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60-63.
25. Giovannoni, S. J., E. F. DeLong, T. M. Schmidt, and N. R. Pace. 1990. Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Appl. Environ. Microbiol. 56:2572-2575.
26. Gordon, L. I., J. C. Jennings, Jr., A. A. Ross, and J. M. Krest. 1994. A suggested protocol for continuous flow automated analysis of seawater nutrients (phosphate, nitrate, nitrite and silicic acid) in the WOCE Hydro-graphic Program and the Joint Global Ocean Fluxes Study. In WOCE operations manual. WOCE report no. 68/91. revision I. WHP Office Report WHPO91-1. Woods Hole Oceanographic Institution, Woods Hole, Mass.
27. Grégori, G., S. Citterio, A. Ghiani, M. Labra, S. Sgorbati, S. Brown, and M. Denis. 2001. Resolution of viable and membrane-compromised bacteria in freshwater and marine waters based on analytical flow cytometry and nucleic acid double staining. Appl. Environ. Microbiol. 67:4662-4670.
28. Huyer, A., R. L. Smith, and J. Fleischbein. 2002. The coastal ocean off Oregon and northern California during the 1997-8 El Niño. Prog. Oceanogr. 54:311-341.
29. Jellett, J. F., W. K. W. Li, P. M. Dickie, A. Boraie, and P. E. Kepkay. 1996. Metabolic activity of bacterioplankton communities assessed by flow cytometry and single carbon substrate utilization. Mar. Ecol. Prog. Ser. 136:213-225.
30. Jochem, F. J. 2001. Morphology and DNA content of baeterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry. Aquat. Micron. Ecol. 25:179-194.
31. Jürgens, K., and H. Güde. 1994. The potential importance of grazing-resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112:169-188.
32. Kirchman, D. L. 2002. The ecology of Cylophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39:91-100.
33. 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.). Current methods in aquatic microbial ecology. Lewis Publishing, New York, N.Y.
34. Kirchman, D. L., L. Yu, and M. T. Cottrell. 2003. Diversity and abundance of uncultured Cytophaga-like bacteria in the Delaware estuary. Appl. Environ. Microbiol. 69:6587-6596.
35. Lebaron, P., P. Servais, H. Agogué, C. Courues, and F. Joux. 2001. Does the high nucleic acid content of individual bacterial cells allow us Io discriminate between active cells and inactive cells in aquatic systems? Appl. Environ. Microbiol. 67:1775-1782.
36. Legendre, L., and J. L. Fèvre, 1995. Microbial food webs and the export of biogenic carbon in oceans. Aquat. Microb. Ecol. 9:69-77.
37. Legendre, L., and F. Rassoulzadegan. 1996. Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Mar. Ecol. Prog. Ser. 145:179-193.
38. Legendre, P., and L. Legendre. 1988. Numerical ecology, 2nd English ed. Elsevier Science BV. Amsterdam, The Netherlands.
39. Li, W. K. W., J. F. Jellett, and P. M. Dickie. 1995. DNA distributions in planktonic bacteria stained with TOTO or TO-PRO. Limnol. Oceanogr. 40:1485-1495.
40. Longnecker, K. 2004. Bacterioplankton in the Oregon upwelling system: distribution, cell-specific leueine incorporation, and diversity. Ph.D. thesis. Oregon State University, Corvallis.
41. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Förster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. König, T. Liss, R. Lüßmann, M. May, B. Nonhoff, B. Reichel, R. Strchlow, A. Stainatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, und K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
42. Malmstrom, R. R., R. P. Kiene, M. T. Cottrell, and D. L. Kirehman. 2004. Contribution of SARH bacteria to dissolved dimecthylsulfoniopropionate and amino acid uptake in the North Atlantic occan. Appl. Environ. Microbiol. 70:4129-4135.
43. Marie, D., F. Partensky, S. Jacquet, and D. Vaulot. 1997. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 63:186-193.
44. Mullins, T. D., T. H. Britschgi, R. L. Krest, and S. J. Giovannoni. 1995. Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific baeterioplankton communities. Limnol. Oceanogr. 40:148-158.
45. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Proliling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
46. Muyzer, G., and K. Smalla. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Leeuwenhoek 73:127-141.
47. Neefs, J.-M., Y. Van De Per, P. De Rijk, S. Chapelle, and R. De Wachter. 1993. Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res. 21:3025-3049.
48. Nielsen, J. L., M. Aquino de Muro, and P. H. Nielsen. 2003. Evaluation ol the redox dye 5-cyano-2.3-tolyl-tetrazolium chloride for activity studies by simultancous use of microautoradiography and fluorescence in situ hybridization. Appl. Environ. Microhiol. 69:641-643.
49. O'Sullivan, L. A., K. E. Fuller, E. M. Thomas, C. M. Turley, J. C. Fry, and A. J. Weightman. 2004. Distribution and culturability of the uncultivated 'agg58' cluster of the Bacteroidetes phylum in aquatic environments. FEMS Microhiol. Ecol. 47:359-370.
50. Pernthaler, A., J. Pernthaler, H. Eilers, and R, Amann. 2001. Growth patterns of two marine isolates: adaptations to substrate patchiness. Appl. Environ. Microbiol. 67:4077-4083.
51. Pernthaler, A., J. Pernthaler, M. Schattenhofer, and R. Amann, 2002. Identification of DNA-synthesizing bacterial cells in coastal North Sea plankton. Appl. Environ. Microhiol. 68:5728-5736.
52. Peterson, W. T., J. E. Keister, and L. R. Feinberg. 2002. The effects of the 1997-1999 El Niño/La Niña events on the hydrography and zooplankton off the central Oregon coast. Prog. Oceanogr. 54:381-398.
53. Rappé, M. S., S. A. Cannon, K. L. Vergin, and S. J. Giovannoni. 2002. Cultivation of the ubiquitous SARI 1 marine bacterioplankton clade. Nature 418:630-633.
54. Rappé, M. S., F. F. Kemp, and S. J. Giovannoni. 1997. Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shell off Cape Hatteras. North Carolina. Limnol. Oceanog. 42:811-826.
55. Rodriguez, G. G., D. Phipps, K. Ishiguro, and H. F. Ridgway. 1992. Use of a fluorescent redox prohe for direct visualization of actively respiring bacteria. Appl. Environ. Microhiol. 58:1801-1808.
56. Schäfer, H., and G. Muyzer. 2001. Denaturing gradient gel electrophoresis in marine microbial ecology, p. 425-468. In J. H. Paul (ed.). Methods in microbiology, vol. 30. Academic Press, San Diego. Calif.
57. Servais, P., H. Agogué, C. Courties, F. Joux, and P. Leharon. 2001. Are the actively respiring cells (CTC +) those responsible for bacterial production in aquatic environments? FEMS Microbiol. Ecol. 35:171-179.
58. Servais, P., E. O. Casamayor, C. Courties, P. Catala, N. Parthuisot, and P. Lebaron. 2003. Activity and diversity of bacterial cells with high and low nucleic acid content. Aquat. Microb. Ecol. 33:41-51.
59. Servais, P., C. Courties, P. Leharon, and M. Troussellier. 1999. Coupling bacterial activity measurements with cell sorting by flow cytometry. Microb. Ecol. 38:180-189.
60. Seymour, J. R., J. G. Mitehell, and L. Seuront. 2004. Microscale beterogeneity in the activity of coastal bacterioplankton communities. Aquat. Microb. Ecol. 35:1-16.
61. Sherr, B. F., P. del Giorgio, and E. B. Sherr. 1999. Estimating abundance and single-cell characteristics of respiring bacteria via the redox dye CTC. Aquat. Microb. Ecol. 18:117-131.
62. Sherr, E. B., B. F. Sherr, and T. J. Cowles. 2001. Mesoscale variability in bacterial activity in the Northeast Pacilie Ocean off Oregon, USA. Aquat. Microb. Ecol. 25:21-30.
63. Sherr, E. B., B. F. Sherr, and P. A. Wheeler. 2005. Distribution of coccoid cyanobacteria and small cukaryotic phytoplankton in the upwelling ecosystem off the Oregon coast during 2001 and 2002. Deep-Sea Res. II 52:317-330.
64. Šimek, K., J. Pernthaler, M. G. Weinbauer, K. Hornák, J. R. Dolan, J. Nedoma, M. Mašíu, and R. Amann. 2001. C banges in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoculrophic reservoir. Appl. Environ. Microhiol. 67:2723-2733.
65. 3H-leucine. Mar. Microb. Food Webs 6:107-114.
66. Smith, E. M. 1998. Coherence of microbial respiration rate and cell-specific bacterial activity in a coastal planklonic community. Aquat. Microb. Ecol. 16:27-35.
67. Smith, E. M., and P. A. del Giorgio. 2003. Low fractions of active bacteria in natural aquatic communities? Aquat. Microh. Ecol. 31:203-208.
68. Smith, J. J., and G. A. McFeters. 1997. Mechanisms of INT (2-(4-iodophenyl)-3-(4-nitrophenyl)-5-phenyl tetrazolium chloride), and CTC (5-cyano-2.3-ditolyl tetrazolium chloride) reduction in Escherichia coli K-12. J. Microbiol. Methods. 29:161-175.
69. Strickland, J. D. H., and T. R. Parsons (ed.). 1972. A practical handbook of seawater analysis. 2nd ed., vol. 167. Fisheries Research Board of Canada, Ottawa. Canada.
70. Troussellier, M., C. Courties, P. Lebaron, and P. Servais. 1999. Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids. FEMS Microbiol. Ecol. 29:319-330.
71. Vaqué, D., E. O. Casamayor, and J. M. Gasol. 2001. Dynamics of whole community haeterial production and grazing losses in seawater incubations as related to the changes in the proportions of bacteria with different DNA content. Aquat. Microb. Ecol. 25:163-177.
72. Wetz, M. S., and P. A. Wheeler. 2004. Response of bacteria to simulated upwelling phytoplankton blooms. Mar. Ecol. Prog. Ser. 272:49-57.
73. Wright, T. D., K. L. Vergin, P. W. Boyd, and S. J. Giovannoni. 1997. A novel δ-subdivision proteobacterial lineage from the lower ocean surface layer. Appl. Environ. Microbiol. 63:1441-1448.
74. Yamaguchi, N., and M. Nasu, 1997. Flow cytometric analysis of bacterial respiratory and enzymatic activity in the natural aquatic environment. J. Appl. Microbiol. 83:43-52.
75. Zubkov, M. V., B. M. Fuchs, S. D. Archer, R. P. Kiene, R. Amann, and P. H. Burkill. 2001. Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionatc in an algal bloom in the North Sea. Environ. Microbiol. 3:304-311.
76. Zuhkov, M. V., B. M. Fuchs, S. D. Archer, R. P. Kiene, R. Amann, and P. H. Hurkill. 2002. Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea. Deep-Sea Res. II 49:3017-3038.
77. Zuhkov, M. V., B. M. Fuehs, P. H. Burkill, and R. Amann. 2001. Comparison of cellular and biomass specific activities of dominant bacterioplankton groups in stratified waters of the Celtic Sea. Appl. Environ. Microbiol. 67:5210-5218.