Single-cell physiological structure and growth rates of heterotrophic bacteria in a temperate estuary (Waquoit Bay, Massachusetts)

Limnology and Oceanography

Volumn 56, Issue 1, 2011, Pages 37-48

  Morán, Xosé Anxelu G ^a,b   Ducklow, Hugh W ^b   Erickson, Matthew ^b  

^a INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^b ECOSYSTEMS CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; ACTIVATION ENERGY; AMINO ACID; BACTERIUM; CYTOCHROME; DISSOLVED ORGANIC CARBON; ESTUARINE ENVIRONMENT; GROWTH RATE; HETEROTROPHY; MEMBRANE; MICROBIAL COMMUNITY; NUCLEIC ACID; PHYSIOLOGICAL RESPONSE; PHYTOPLANKTON; TEMPERATE ENVIRONMENT;

MASSACHUSETTS; UNITED STATES; WAQUOIT BAY;

BACTERIA (MICROORGANISMS);

EID: 78651402334     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2011.56.1.0037     Document Type: Article

References (79)

1. Alonso-SÁez, L., J. M. Gasol, T.Lefort, J.Hofer, and R. Sommaruga. 2006. Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl. Environ. Microbiol. 72: 5806-5813 doi:10.1128/AEM.00597-06
2. -, and others. 2008. Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system. Ecosystems 11: 397-109 doi:10.1007/s10021-008-9129-0
3. Beardsley, C., J. Pernthaler, W.Wosniok, and R. Amann. 2003. Are readily culturable bacteria in coastal North Sea waters suppresed by selective grazing mortality? Appl. Environ. Microbiol. 69: 2624-2630 doi:10.1128/AEM.69.5.2624- 2630.2003
4. Belzile, C., S. Brugel, C.Nozais, Y.Gratton, and S. Demers. 2008. Variations of the abundance and nucleic acid content of heterotrophic bacteria in Beaufort Shelf waters during winter and spring. J. Mar. Sys. 74: 946-956 doi:10.1016/j.jmarsys. 2007.12.010
5. Bonilla-Findji, O., A. Malits, D.LefÉvre, E. Rochelle- Newall, R.LemÉe, M. G. Weinbauer, and J.-P. Gattuso. 2008. Viral effects on bacterial respiration, production and growth efficiency: Consistent trends in the Southern Ocean and the Mediterranean Sea. Deep-Sea Res. II 55: 790-800 doi:10.1016/j.dsr2.2007.12.004
6. Bouvier, T., P. A. Del Giorgio, and J. M. Gasol. 2007. A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environ. Microbiol. 9: 2050-2066 doi:10.1111/j.1462-2920.2007.01321.x
7. Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and G. B. West. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771-1789 doi:10.1890/03-9000
8. Calvo-Díaz, A., and X. A. G. MorÁn.2009. Empirical leucine-to- carbon conversion factors for estimating heterotrophic bacterial production: seasonality and predictability in a temperate coastal ecosystem. Appl. Environ. Microbiol. 75: 3216-3221 doi:10.1128/AEM.01570-08
9. CARLSON, C.A., AND H. W.DUCKLOW. 1996. Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat. Microb. Ecol. 10: 69-85, doi:10.3354/ame010069
10. Choi, J. W., B. F. Sherr, and E. B. Sherr. 1999. Dead or alive? A large fraction of ETS-inactive marine bacterioplankton cells, as assessed by reduction of CTC, can become ETS-active with incubation and substrate addition. Aquat. Microb. Ecol. 18: 105-115 doi:10.3354/ame018105
11. Church, M. J. 2008. Resource control of bacterial dynamics in the sea, p. 335-382. In D. L. Kirchman [ed.], Microbial ecology of the oceans, 2nd ed. Wiley-Liss.
12. Comte, J., and P. A. Del Giorgio. 2009. Links between resources, C metabolism and the major components of bacterioplankton community structure across a range of freshwater ecosystems. Environ. Microbiol. 11: 1704-1716 doi:10.1111/j.1462-2920. 2009.01897.x
13. Corzo, A., S. RodrÍguez-GÁlvez, L. Lubian, C. Sobrino, P. Sangrá, and A. Martínez. 2005. Antarctic marine bacterio- plankton subpopulations discriminated by their apparent content of nucleic acids differ in their response to ecological factors. Polar Biol. 29: 27-39 doi:10.1007/s00300-005-0032-2
14. Del Giorgio, P. A., and T. C. Bouvier. 2002. Linking the physiologic and phylogenetic successions in free-living bacterial communities along an estuarine salinity gradient. Limnol. Oceanogr. 47: 471-486 doi:10.4319/lo.2002.47.2.0471
15. -, and J. M. Gasol. 2008. Physiological structure and single-cell activity in marine bacterioplankton, p. 243-298. In D. L. Kirchman [ed.], Microbial ecology of the oceans, 2nd ed. Wiley-Liss.
16. -, -, D. Vaqué, P. Mura, S. Agustí, and C. M. Duarte. 1996. Bacterioplankton community structure: Protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. oceanogr. 41: 1169-1179 doi:10.4319/lo.1996.41.6.1169
17. -, Y. T. PRAIRIE, AND D. F. BIRD. 1997. Coupling between rates of bacterial production and the abundance of metabolically active bacteria in lakes, enumerated using CTC reduction and flow cytometry. Microb. Ecol. 34: 144-154, doi:10.1007/s002489900044
18. Ducklow, H. 2000. Bacterial production and biomass in the oceans, p. 85-120. In D. L. Kirchman [ed.], Microbial ecology of the oceans. Wiley-Liss.
19. -, C. Carlson, M.Church, D. Kirchman, D. Smith, and G. Steward. 2001. The seasonal development of the bacterioplankton bloom in the Ross Sea, Antarctica, 1994-1997. Deep-Sea Res. II 48: 4199-1221 doi:10.1016/S0967-0645(01)00086-8
20. -, -, and W. Smith. 1999. Bacterial growth in experimental plankton assemblages and seawater cultures from the Phaeocystis antárctica bloom in the Ross Sea, Antarctica. Aquat. Microb. Ecol. 19: 215-227 doi:10.3354/ame019215
21. -, X. A. G. MorÁn, and A. E. Murray. 2010. Bacteria in the greenhouse: Marine microbes and climate change, p. 1-31. In R. Mitchell and J. D. Gu [eds.], Environmental microbiology, 2nd ed. Wiley-Blackwell.
22. Ellis-Evans, J. C., V. Galchenko, J. Laybourn-Parry, A. P. Mylnikov, and W. Petz. 2001. Environmental characteristics and microbial plankton activity of freshwater environments at Kongsfjorden, Spitsbergen (Svalbard). Archiv Hydrobiol. 152: 609-632.
23. Feuerpfeil, P., and others. 2004. Carbon budget and pelagic community compositions at two coastal areas that differ in their degree of eutrophication, in the southern Baltic sea. Estuar. Coast. Shelf Sci. 61: 89-100 doi:10.1016/j.ecss.2004.04.006
24. Findlay, S., M. L. Pace, D.Lints, J. J.Cole, N. F. Caraco, and B. Peierls. 1991. Weak coupling of bacterial and algal production in a heterotrophic ecosystem: The Hudson River estuary. Limnol. Oceanogr. 36: 268-278 doi:10.4319/lo. 1991.36.2.0268
25. 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 doi:10.1046/j.1462-2920.2000.00092.x
26. Gasol, J. M., and J. Aristegui. 2007. Cytometric evidence reconciling the toxicity and usefulness of CTC as a marker of bacterial activity. Aquat. Microb. Ecol. 46: 71-83 doi:10.3354/ame046071
27. -, P. A. Del Giorgio, R. Massana, and C. M. Duarte. 1995. Active versus inactive bacteria: Size-dependence in coastal marine plankton community. Mar. Ecol. Prog. Ser. 128: 91-97 doi:10.3354/meps128091
28. -, and X. A. G. Morán. 1999. Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquat. Microb. Ecol. 16: 251-264 doi:10.3354/ame016251
29. -, U. L. Zweifel, F. Peters, J. A. Fuhrman, and A. Hagström. 1999. Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl. Environ. Microbiol. 65: 4475-4483.
30. Gillooly, J. F., J. H. Brown, G.B.West, V.M.Savage, and E. L. Charnov. 2001. Effects of size and temperature on metabolic rate. Science 293: 2248-2251 doi:10.1126/science. 1061967
31. 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 doi:10.1128/AEM.67.10. 4662-4670.2001
32. Hoch, M. P., and D. L. Kirchman. 1993. Seasonal and interannual variability in bacterial production and biomass in a temperate estuary. Mar. Ecol. Prog. Ser. 98: 283-295 doi:10.3354/meps098283
33. Jochem, F. J., P. J. Lavrentyev, and M. R. First. 2004. Growth and grazing rates of bacteria groups with different apparent DNA content in the Gulf of Mexico. Mar. Biol. 145: 1213-1225 doi:10.1007/s00227-004-1406-7
34. 2 fixation of chemolithoautotrophic prokaryotes in anoxic waters of the Baltic Sea. Limnol. Oceanogr. 53: 14-22.
35. Joux, F., P. Servais, J. J.Naudin, P. Lebaron, L. Oriol, and C. Courties. 2005. Distribution of picophytoplankton and bacterioplankton along a river plume gradient in the Mediterranean Sea. Vie Milieu-Life Environ. 55: 197-208.
36. KAhler, P., P. K. Bjørnsen, K. Lochte, and A. Antia. 1997. Dissolved organic matter and its utilization by bacteria during spring in the Southern Ocean. Deep-Sea Res. II 44: 341-353 doi:10.1016/S0967-0645(96)00071-9
37. Kirchman, D. L. 2002. Calculating microbial growth rates from data on production and standing stocks. Mar. Ecol. Prog. Ser. 233: 303-306 doi:10.3354/meps233303
38. -, E. K'nees, and R. Hodson. 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl. Environ. Microbiol. 49: 599-607.
39. -, X. A. G. Morán, and H. Ducklow. 2009. Microbial growth in the polar oceans role of temperature and potential impact of climate change. Nature Rev. Microbiol. 7: 451-459.
40. -, J. H. Rich, and R. T. Barber. 1995. Biomass and biomass production of heterotrophic bacteria along 140°Win the equatorial Pacific: Effect of temperature on the microbial loop. Deep-Sea Res. II 42: 603-619 doi:10.1016/0967-0645 (95)00021-H
41. Lamy, D., L. F. Artigas, C. Jauzein, F. Lizon, and V. Cornille. 2006. coastal bacterial viability and production in the eastern English Channel: A case study during a Phaeocystis globosa bloom. J. Sea Res. 56: 227-238 doi:10.1016/j.seares.2006.04.003
42. 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 doi:10.4319/lo.1995.40.8.1485
43. Longnecker, K., B. F. Sherr, and E. B. Sherr. 2005. 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 doi:10.1128/AEM.71.12.7737-7749.2005
44. Lopez-Urrutia, Á., and X. A. G. Morán. 2007. Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88: 817-822 doi:10.1890/06-1641
45. -, E. San Martin, R.P.Harris, and X. Irigoien. 2006. Scaling the metabolic balance of the oceans. Proc. Nat. Acad. Sci. USA 103: 8739-8744 doi:10.1073/pnas.0601137103
46. Lovejoy, C., L. Legendre, B. Klein, J. E. Tremblay, R. G. Ingram, and J. C. Therriault. 1996. Bacterial activity during early winter mixing (Gulf of St. Lawrence, Canada). Aquat. Microb. Ecol. 10: 1-13 doi:10.3354/ame010001
47. Mary, I., J. L. Heywood, B. M. Fuchs, R. Amann, G. A. Tarran, P. H. Burkill, and M. V. Zubkov. 2006. SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat. Microb. Ecol. 45: 107-113 doi:10.3354/ame045107
48. MorÁn, X. A. G., A. Bode, L.Á.SuÁrez, and E. Nogueira. 2007. Assessing the relevance of nucleic acid content as an indicator of marine bacterial activity. Aquat. Microb. Ecol. 46: 141-152 doi:10.3354/ame046141
49. -, and A. Calvo-Diaz. 2009. Single-cell vs. bulk activity properties of coastal bacterioplankton over an annual cycle in a temperate ecosystem. FEMS Microbiol. Ecol. 67: 43-56 doi:10.1111/j.1574-6941.2008.00601.x
50. -, -, and H. W. Ducklow. 2010. Total and phytoplankton mediated bottom-up control of bacterioplankton change with temperature in NE Atlantic shelf waters. Aquat. Microb. Ecol. 58: 229-239 doi:10.3354/ame01374
51. -, M. Estrada, J. M. Gasol, and C. PedrOs-AliO. 2002a. Dissolved primary production and the strength of phytoplank- ton bacterioplankton coupling in contrasting marine regions. Microb. Ecol. 44: 217-223 doi:10.1007/s00248-002- 1026-z
52. -, J. M. Gasol, C. PedrÓs-AliÓ, and M. Estrada. 2002b. Partitioning of phytoplanktonic organic carbon production and bacterial production along a coastal-offshore gradient in the NE Atlantic during different hydrographic regimes. Aquat. Microb. Ecol. 29: 239-252 doi:10.3354/ame029239
53. PedrÓs-AliÓ, C., D. VaquÉ, N. Guixa-Boixereu, and J. M. Gasol. 2002. Prokaryotic plankton biomass and heterotrophic production in western Antarctic waters during the 1995- 1996 Austral summer. Deep-Sea Res. II 49: 805-825 doi:10.1016/S0967-0645(01)00125-4
54. Revilla, M., A. Iriarte, I. Madariaga, and E. Orive. 2000. Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary. Estuar. Coast. Shelf Sci. 50: 297-313 doi:10.1006/ecss.1999.0576
55. Rodriguez, G. G., D. Phipps, K. Ishiguro, and H. F. Ridgway. 1992. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol. 58: 1801-1808.
56. Scharek, R., and M. Latasa. 2007. Growth, grazing and carbon flux of high and low nucleic acid bacteria differ in surface and deep chlorophyll maximum layers in the NW Mediterranean Sea. Aquat. Microb. Ecol. 46:153-161 doi:10.3354/ame046153
57. Schumann, R., U. Schiewer, U. Karsten, and T. Rieling. 2003. viability of bacteria from different aquatic habitats. ii. Cellular fluorescent markers for membrane integrity and metabolic activity. Aquat. Microb. Ecol. 32: 137-150 doi:10.3354/ame032137
58. 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 doi:10.3354/ame018117
59. Sherr, E. B., B. F. Sherr, and K. Longnecker. 2006. Distribution of bacterial abundance and cell specific nucleic acid content in the northeast Pacific Ocean. Deep-Sea Res. I 53: 713-725 doi:10.1016/j.dsr.2006.02.001
60. Shiah, F. K., and H. W. Ducklow. 1994a. Temperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, USA. Mar. Ecol. Prog. Ser. 103: 297-308 doi:10.3354/meps103297
61. -, and-. 1994b. Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth-rate in Chesapeake Bay. Limnol. Oceanogr. 39: 1243-1258 doi:10.4319/lo.1994.39.6.1243
62. Smith, D. C., and F. Azam. 1992. A simple, economical method for measuring bacterial protein synthesis rates in sea water using 3H-leucine. Mar. Microb. Food Webs 6: 107-114.
63. Smith, E. M. 1998. Coherence of microbial respiration rate and cell-specific bacterial activity in a coastal planktonic community. Aquat. Microb. Ecol. 16: 27-35 doi:10.3354/ame016027
64. -, and P. A. Del Giorgio. 2003. Low fractions of active bacteria in natural aquatic communities? Aquat. Microb. Ecol. 31: 203-208 doi:10.3354/ame031203
65. Søndergaard, M., and M. Danielsen. 2001. Active bacteria (CTC+) in temperate lakes: Temporal and cross-system variations. J. Plankt. Res. 23: 1195-1206 doi:10.1093/plankt/23.11.1195
66. Staroscik, A. M., and D. C. Smith. 2004. Seasonal patterns in bacterioplankton abundance and production in Narragansett Bay, Rhode Island, USA. Aquat. Microb. Ecol. 35: 275-282 doi:10.3354/ame035275
67. Steinberg, D. K., C. A. Carlson, N. R. Bates, R.J. Johnson, A.F. Michaels, and A. H. Knap. 2001. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): A decade-scale look at ocean biology and biogeochemistry. Deep-Sea Res. II 48: 1405-1447 doi:10.1016/S0967-0645(00)00148- X
68. Teira, E., S. Martínez-Garcia, C.Lønborg, and X. A. Álvarez- Salgado. 2009. Growth rates of different phylogenetic bacterio-plankton groups in a coastal upwelling system. Environ. Microbiol. Rep. 1: 545-554 doi:10.1111/j.1758-2229.2009.00079.x
69. Valiela, I., and others. 1992. Couplings of watersheds and coastal waters: Sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15: 443-157.
70. VaquÉ, D., E. O. Casamayor, and J. M. Gasol. 2001. Dynamics of whole community bacterial 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 doi:10.3354/ame025163
71. Wang, Y. Y., F. Hammes, N. Boon, M. Chami, and T. Egli. 2009. Isolation and characterization of low nucleic acid (LNA)- content bacteria. ISME J. 3: 889-902 doi:10.1038/ismej.2009.46
72. 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: 99-118 doi:10.1007/BF02539147
73. Wright, R. T., and R. B. Coffin. 1983. Planktonic bacteria in estuaries and coastal waters of northern Massachusetts: Spatial and temporal distribution. Mar. Ecol. Prog. Ser. 11: 205-216 doi:10.3354/meps011205
74. Yager, P. L., and others. 2001. Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol. Oceanogr. 46: 790-801 doi:10.4319/lo.2001.46.4.0790
75. Yokokawa, T., and T. Nagata. 2005. Growth and grazing mortality rates of phylogenetic groups of bacterioplankton in coastal marine environments. Appl. Environ. Microbiol. 71: 6799-6807 doi:10.1128/AEM.71.11.6799-6807.2005
76. -, -, M. T. Cottrell, and D. L. Kirchman. 2004. Growth rate of the major phylogenetic bacterial groups in the Delaware estuary. Limnol. Oceanogr. 49: 1620-1629 doi:10.4319/lo.2004.49.5.1620
77. Zöllner, E., H. G. Hoppe, U.Sommer, and K. JÜrgens. 2009. Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnol. Oceanogr. 54: 262-275.
78. Zubkov, M. V., J. I. Allen, and B. M. Fuchs. 2004. Coexistence of dominant groups in marine bacterioplankton community-a combination of experimental and modelling approaches. J. Mar. Biol. Ass. UK 84: 519-529 doi:10.1017/S002531540400952Xh
79. -, B. M. Fuchs, 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 doi:10.1128/AEM.67.11.5210-5218.2001