A comparative study of the cytometric characteristics of High and Low nucleic-acid bacterioplankton cells from different aquatic ecosystems

Environmental Microbiology

Volumn 9, Issue 8, 2007, Pages 2050-2066

  Bouvier, Thierry ^a   Del Giorgio, Paul A ^b   Gasol, Josep M ^c  

^a UNIV MONTPELLIER   (France)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^c INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEIC ACID;

ARTICLE; BACTERIUM; CHEMISTRY; COMPARATIVE STUDY; ECOSYSTEM; FLOW CYTOMETRY; MICROBIOLOGY; PLANKTON;

BACTERIA; ECOSYSTEM; FLOW CYTOMETRY; NUCLEIC ACIDS; PLANKTON; WATER MICROBIOLOGY;

EID: 34447327017     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01321.x     Document Type: Article

References (63)

1. Åkerlund, T., Nordstrom, K. Bernander, R. (1995) Analysis of cell-size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia-coli. J Bacteriol 177 : 6791 6797.
2. Andreatta, S., Wallinger, M.M., Piera, J., Catalan, J., Psenner, R., Hofer, J.S. Sommaruga, R. (2004) Tools for discrimination and analysis of lake bacterioplankton subgroups measured by flow cytometry in a high-resolution depth profile. Aquat Microb Ecol 36 : 107 115.
3. Bernard, L., Schafer, H., Joux, F., Courties, C., Muyzer, G. Lebaron, P. (2000) Genetic diversity of total, active and culturable marine bacteria in coastal seawater. Aquat Microb Ecol 23 : 1 11.
4. Binder, B.J. Chisholm, S.W. (1995) Cell cycle regulation in marine Synechococcus sp. strains. Appl Environ Microbiol 61 : 708 717.
5. Bouvier, T., Troussellier, M., Anzil, A., Courties, C. Servais, P. (2001) Using light scatter signal to estimate bacterial bioVolume by flow cytometry. Cytometry 44 : 188 194.
6. Brussaard, C.P.D., Thyrhaug, R., Marie, D. Bratbak, G. (1999) Flow cytometric analyses of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). J Phycol 35 : 941 948.
7. Button, D.K. Robertson, B.R. (1989) Kinetics of bacterial processes in natural aquatic systems based on biomass as determined by high-resolution flow-cytometry. Cytometry 10 : 558 563.
8. Button, D.K. Robertson, B.R. (2001) Determination of DNA content of aquatic bacteria by flow cytometry. Appl Environ Microbiol 67 : 1636 1645.
9. Button, D.K., Robertson, B.R. Juttner, F. (1996) Microflora of a subalpine lake: bacterial populations, size and DNA distributions, and their dependence on phosphate. FEMS Microbiol Ecol 21 : 87 101.
10. Button, D.K., Robertson, B.R., Lepp, P.W. Schmidt, T.M. (1998) A small, dilute-cytoplasm, high-affinity, novel bacterium isolated by extinction culture and having kinetic constants compatible with growth at ambient concentrations of dissolved nutrients in seawater. Appl Environ Microbiol 64 : 4467 4476.
11. Calvo-Díaz, A. Morán, X.A.G. (2006) Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay. Aquat Microb Ecol 42 : 159 174.
12. Christensen, H., Bakken, L.R. Olsen, R.A. (1993) Soil bacterial-DNA and biovolume profiles measured by flow-cytometry. FEMS Microbiol Ecol 102 : 129 140.
13. Christensen, H., Olsen, R.A. Bakken, L.R. (1995) Flow cytometric measurements of cell volumes and DNA contents during culture of indigenous soil bacteria. Microb Ecol 29 : 49 62.
14. Corzo, A., Rodríguez-Gálvez, S., Lubían, L., Sobrino, C., Sangrá, P. Martínez, A. (2005) Antarctic marine bacterioplankton subpopulations discriminated by their apparent content of nucleic acids differ in their response to ecological factors. Polar Biol 29 : 27 39.
15. DeBruijn, F.J., Lupiski, J.R. Weinstock, G. (1997) Bacterial Genomes: Physical Structure and Analysis. New York, USA : New York Chapman & Hall.
16. Eilers, H., Pernthaler, J. Amann, R. (2000) Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Appl Environ Microbiol 66 : 4634 4640.
17. Fuchs, B.M., Zubkov, M.V., Sahm, K., Burkill, P.H. Amann, R. (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.
18. Fuchs, B.M., Woebken, D., Zubkov, M.V., Burkill, P. Amann, R. (2005) Molecular identification of picoplankton populations in contrasting waters of the Arabian Sea. Aquat Microb Ecol 39 : 145 157.
19. Gasol, J.M. del Giorgio, P.A. (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 64 : 197 224.
20. Gasol, J.M., Zweifel, U.L., Peters, F., Fuhrman, J.A. Hagstrom, A. (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microbiol 65 : 4475 4483.
21. del Giorgio, P.A., Bird, D.F., Prairie, Y.T. Planas, D. (1996) Flow cytometric determination of bacterial abundance in lake plankton with the green nucleic acid stain SYTO 13. Limnol Oceanogr 41 : 783 789.
22. Glöckner, F.O., Fuchs, B.M. Amann, R. (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65 : 3721 3726.
23. Guindulain, T. Vives-Rego, J. (2002) Involvement of RNA and DNA in the staining of Escherichia coli by SYTO 13. Lett Appl Microbiol 34 : 182 188.
24. Hood, M.A., guckert, J.B., White, D.C. Deck, F. (1986) Effect of nutrient depravation on lipid, carbohydrate, DNA, RNA, and protein levels in Vibrio cholerae. Appl Environ Microbiol 52 : 788 793.
25. Islas, S., Becerra, A., Luisi, P.L. Lazcano, A. (2004) Comparative genomics and the gene complement of a minimal cell. Orig Life Evol Biosph 34 : 243 256.
26. Jeffrey, W.H., Nazaret, S. Barkay, T. (1996) Detection of the merA gene and its expression in the environment. Microb Ecol 32 : 293 303.
27. Jellett, J.F., Li, W.K.W., Dickie, P.M., Boraie, A. Kepkay, P.E. (1996) Metabolic activity of bacterioplankton communities assessed by flow cytometry and single carbon substrate utilization. Mar Ecol Prog Ser 136 : 213 225.
28. Jochem, F.J. (2001) Morphology and DNA content of bacterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry. Aquat Microb Ecol 25 : 179 194.
29. Jochem, F.J., Lavrentyev, P.J. First, M.R. (2004) Growth and grazing rates of bacteria groups with different apparent DNA content in the Gulf of Mexico. Mar Biol 145 : 1213 1225.
30. Joux, F., Lebaron, P. Troussellier, M. (1997) Succession of cellular states in a Salmonella typhimurium population during starvation in artificial seawater microcosms. FEMS Microbiol Ecol 22 : 65 76.
31. Joux, F., Jeffrey, W.H., Lebaron, P. Mitchell, D.L. (1999) Marine bacterial isolates display diverse responses to UV-B radiation. Appl Environ Microbiol 65 : 3820 3827.
32. Kirchman, D.L. (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In Handbook of Methods in Aquatic Microbial Ecology. Kemp, P.F., Sherr, B.F., Sherr, E.B. Cole, J.J. (eds). Danvers, USA : Lewis, pp. 509 512.
33. Lebaron, P. Joux, F. (1994) Flow cytometric analysis of the cellular DNA content of salmonella-typhimurium and alteromonas-haloplanktis during starvation and recovery in seawater. Appl Environ Microbiol 60 : 4345 4350.
34. Lebaron, P., Parthuisot, N. Catala, P. (1998) Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems. Appl Environ Microbiol 64 : 1725 1730.
35. Lebaron, P., Servais, P., Agogue, H., Courties, C. Joux, F. (2001a) Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 67 : 1775 1782.
36. Lebaron, P., Servais, P., Troussellier, M., Courties, C., Muyzer, G., Bernard, L., et al. (2001b) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in abundances, activity and composition. FEMS Microbiol Ecol 34 : 255 266.
37. Lebaron, P., Servais, P., Baudoux, A.C., Bourrain, M., Courties, C. Parthuisot, N. (2002) Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aquat Microb Ecol 28 : 131 140.
38. Legendre, L., Courties, C. Troussellier, M. (2001) Flow cytometry in oceanography 1989-99: environmental challenges and research trends. Cytometry 44 : 164 172.
39. Li, W.K.W. (1990) Bivariate and trivariate analysis in flow-cytometry - phytoplankton size and fluorescence. Limnol Oceanogr 35 : 1356 1368.
40. Li, W.K.W., Jellett, J.F. Dickie, P.M. (1995) DNA distributions in planktonic bacteria stained with TOTO or TO-PRO. Limnol Oceanogr 40 : 1485 1495.
41. Longnecker, K., Sherr, E.B. Sherr, B.F. (2005a) Activity and phylogenetic diversity of high and low nucleic acid content, and ETS-active, bacterial cells in an upwelling ecosystem. Appl Environ Microbiol 71 : 7737 7749.
42. Longnecker, K., Sherr, B.F. Sherr, E.B. (2005b) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Appl Environ Microbiol 71 : 7737 7749.
43. Longnecker, K., Sherr, B.F. Sherr, E.B. (2006) Variation in cell-specific rates of leucine and thymidine incorporation by marine bacteria with high and with low nucleic acid content off the Oregon coast. Aquat Microb Ecol 43 : 113 125.
44. Marie, D., Partensky, F., Jacquet, S. Vaulot, D. (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.
45. Mary, I., Heywood, J.L., Fuchs, B.M., Amann, R., Tarran, G.A., Burkill, P.H. Zubkov, M.V. (2006) SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat Microb Ecol 45 : 107 113.
46. Morán, X.A.G., Bode, A., Suárez, L.A. Nogueira, E. (2007) Assessing the relevance of nucleic acid content as an indicator of marine bacterial activity. Aquat Microb Ecol 46 : 141 152.
47. Nilsson, A.I., Koskiniemi, S., Eriksson, S., Kugelberg, E., Hinton, J.C.D. Andersson, D.I. (2005) Bacterial genome size reduction by experimental evolution. Proc Natl Acad Sci USA 102 : 12112 12116.
48. Nishimura, Y., Kim, C. Nagata, T. (2005) Vertical and seasonal variations of bacterioplankton subgroups with different nucleic acid contents: possible regulation by phosphorus. Appl Environ Microbiol 71 : 5828 5836.
49. Porter, J. Pickup, R.W. (2000) Nucleic acid-based fluorescent probes in microbial ecology: application of flow cytometry. J Microbiol Methods 42 : 75 79.
50. Robertson, B.R. Button, D.K. (1989) Characterizing aquatic bacteria according to population, cell-size, and apparent DNA content by flow-cytometry. Cytometry 10 : 70 76.
51. Robertson, B.R., Button, D.K. Koch, A.L. (1998) Determination of the biomasses of small bacteria at low concentrations in a mixture of species with forward light scatter measurements by flow cytometry. Appl Environ Microbiol 64 : 3900 3909.
52. Servais, P., Casamayor, E.O., Courties, C., Catala, P., Parthuisot, N. Lebaron, P. (2003) Activity and diversity of bacterial cells with high and low nucleic acid content. Aquat Microb Ecol 33 : 41 51.
53. Seymour, J.R., Seuront, L. Mitchell, J.G. (2005) Microscale and small-scale temporal dynamics of a coastal planktonic microbial community. Mar Ecol Prog Ser 300 : 21 37.
54. Sherr, E.B., Sherr, B.F. Longnecker, K. (2006) Distribution of bacterial abundance and cell-specific nucleic acid content in the Northeast Pacific Ocean. Deep Sea Res Part I Oceanogr Res Pap 53 : 713 725.
55. Smith, D.C. Azam, F. (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6 : 107 114.
56. Steen, H.B. (2002) A sample injection device for flow cytometers. Cytometry 49 : 70 72.
57. Steen, H.B., Boye, E. Godal, T. (1981) Applications of flow-cytometry of bacteria. Cytometry 2 : 128 129.
58. Troussellier, M., Courties, C., Lebaron, P. Servais, P. (1999) Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids. FEMS Microbiol Ecol 29 : 319 330.
59. Yanada, M., Yokokawa, T., Lee, C.W., Tanaka, H., Kudo, I. Maita, Y. (2000) Seasonal variation of two different heterotrophic bacterial assemblages in subarctic coastal seawater. Mar Ecol Prog Ser 204 : 289 292.
60. Zubkov, M.V. Tarran, G.A. (2005) Amino acid uptake of Prochlorococcus spp. in surface waters across the South Atlantic Subtropical Front. Aquat Microb Ecol 40 : 241 249.
61. Zubkov, M.V., Fuchs, B.M., Burkill, P.H. Amann, R. (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.
62. Zubkov, M.V., Fuchs, B.M., Tarran, G.A., Burkill, P.H. Amann, R. (2002) Mesoscale distribution of dominant bacterioplankton groups in the northern North Sea in early summer. Aquat Microb Ecol 29 : 135 144.
63. Zubkov, M.V., Tarran, G.A. Burkill, P.H. (2006) Bacterioplankton of low and high DNA content in the suboxic waters of the Arabian Sea and the Gulf of Oman: abundance and amino acid uptake. Aquat Microb Ecol 43 : 23 32.