This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Eilers, H.
Right arrow Articles by Amann, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Eilers, H.
Right arrow Articles by Amann, R.
Agricola
Right arrow Articles by Eilers, H.
Right arrow Articles by Amann, R.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, July 2000, p. 3044-3051, Vol. 66, No. 7
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Culturability and In Situ Abundance of Pelagic Bacteria from the North Sea

Heike Eilers, Jakob Pernthaler,* Frank Oliver Glöckner, and Rudolf Amann

Max-Planck-Institut für marine Mikrobiologie, D-28359 Bremen, Germany

Received 9 March 2000/Accepted 28 April 2000

The culturability of abundant members of the domain Bacteria in North Sea bacterioplankton was investigated by a combination of various cultivation strategies and cultivation-independent 16S rRNA-based techniques. We retrieved 16S rRNA gene (rDNA) clones from environmental DNAs and determined the in situ abundance of different groups and genera by fluorescence in situ hybridization (FISH). A culture collection of 145 strains was established by plating on oligotrophic medium. Isolates were screened by FISH, amplified ribosomal DNA restriction analysis (ARDRA), and sequencing of representative 16S rDNAs. The majority of isolates were members of the genera Pseudoalteromonas, Alteromonas, and Vibrio. Despite being readily culturable, they constituted only a minor fraction of the bacterioplankton community. They were not detected in the 16S rDNA library, and FISH indicated rare (<1% of total cell counts) occurrence as large, rRNA-rich, particle-associated bacteria. Conversely, abundant members of the Cytophaga-Flavobacteria and gamma proteobacterial SAR86 clusters, identified by FISH as 17 to 30% and up to 10% of total cells in the North Sea bacterioplankton, respectively, were cultured rarely or not at all. Whereas SAR86-affiliated clones dominated the 16S rDNA library (44 of 53 clones), no clone affiliated to the Cytophaga-Flavobacterum cluster was retrieved. The only readily culturable abundant group of marine bacteria was related to the genus Roseobacter. The group made up 10% of the total cells in the summer, and the corresponding sequences were also present in our clone library. Rarefaction analysis of the ARDRA patterns of all of the isolates suggested that the total culturable diversity by our method was high and still not covered by the numbers of isolated strains but was almost saturated for the gamma proteobacteria. This predicts a limit to the isolation of unculturable marine bacteria, particularly the gamma-proteobacterial SAR86 cluster, as long as no new techniques for isolation are available and thus contrasts with more optimistic accounts of the culturability of marine bacterioplankton.


* Corresponding author. Mailing address: Max-Planck-Institut für marine Mikrobiologie, Celsiusstrasse 1, D-28359 Bremen, Germany. Phone: 49 421 2028 940. Fax: 49 421 2028 580. E-mail: jperntha{at}mpi-bremen.de.


Applied and Environmental Microbiology, July 2000, p. 3044-3051, Vol. 66, No. 7
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Santos, A. L., Mendes, C., Gomes, N. C. M., Henriques, I., Correia, A., Almeida, A., Cunha, A. (2009). Short-term variability of abundance, diversity and activity of estuarine bacterioneuston and bacterioplankton. J PLANKTON RES 31: 1545-1555 [Abstract] [Full Text]  
  • Oh, H.-M., Giovannoni, S. J., Lee, K., Ferriera, S., Johnson, J., Cho, J.-C. (2009). Complete Genome Sequence of Robiginitalea biformata HTCC2501. J. Bacteriol. 191: 7144-7145 [Abstract] [Full Text]  
  • Weon, H.-Y., Son, J.-A, Yoo, S.-H., Hong, S.-B., Jeon, Y.-A., Kwon, S.-W., Koo, B.-S. (2009). Rubellimicrobium aerolatum sp. nov., isolated from an air sample in Korea. Int. J. Syst. Evol. Microbiol. 59: 406-410 [Abstract] [Full Text]  
  • Allers, E., Niesner, C., Wild, C., Pernthaler, J. (2008). Microbes Enriched in Seawater after Addition of Coral Mucus. Appl. Environ. Microbiol. 74: 3274-3278 [Abstract] [Full Text]  
  • Meyer, B., Kuever, J. (2007). Molecular Analysis of the Diversity of Sulfate-Reducing and Sulfur-Oxidizing Prokaryotes in the Environment, Using aprA as Functional Marker Gene. Appl. Environ. Microbiol. 73: 7664-7679 [Abstract] [Full Text]  
  • Ying, J.-Y., Wang, B.-J., Dai, X., Yang, S.-S., Liu, S.-J., Liu, Z.-P. (2007). Wenxinia marina gen. nov., sp. nov., a novel member of the Roseobacter clade isolated from oilfield sediments of the South China Sea. Int. J. Syst. Evol. Microbiol. 57: 1711-1716 [Abstract] [Full Text]  
  • Alonso-Saez, L., Gasol, J. M. (2007). Seasonal Variations in the Contributions of Different Bacterial Groups to the Uptake of Low-Molecular-Weight Compounds in Northwestern Mediterranean Coastal Waters. Appl. Environ. Microbiol. 73: 3528-3535 [Abstract] [Full Text]  
  • Hamasaki, K., Taniguchi, A., Tada, Y., Long, R. A., Azam, F. (2007). Actively Growing Bacteria in the Inland Sea of Japan, Identified by Combined Bromodeoxyuridine Immunocapture and Denaturing Gradient Gel Electrophoresis. Appl. Environ. Microbiol. 73: 2787-2798 [Abstract] [Full Text]  
  • Sapp, M., Wichels, A., Gerdts, G. (2007). Impacts of Cultivation of Marine Diatoms on the Associated Bacterial Community. Appl. Environ. Microbiol. 73: 3117-3120 [Abstract] [Full Text]  
  • Fuchs, B. M., Spring, S., Teeling, H., Quast, C., Wulf, J., Schattenhofer, M., Yan, S., Ferriera, S., Johnson, J., Glockner, F. O., Amann, R. (2007). From the Cover: Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc. Natl. Acad. Sci. USA 104: 2891-2896 [Abstract] [Full Text]  
  • Eiler, A. (2006). Evidence for the Ubiquity of Mixotrophic Bacteria in the Upper Ocean: Implications and Consequences. Appl. Environ. Microbiol. 72: 7431-7437 [Full Text]  
  • Sintes, E., Herndl, G. J. (2006). Quantifying Substrate Uptake by Individual Cells of Marine Bacterioplankton by Catalyzed Reporter Deposition Fluorescence In Situ Hybridization Combined with Microautoradiography. Appl. Environ. Microbiol. 72: 7022-7028 [Abstract] [Full Text]  
  • Eiler, A., Johansson, M., Bertilsson, S. (2006). Environmental Influences on Vibrio Populations in Northern Temperate and Boreal Coastal Waters (Baltic and Skagerrak Seas). Appl. Environ. Microbiol. 72: 6004-6011 [Abstract] [Full Text]  
  • Dai, X., Wang, B.-J., Yang, Q.-X., Jiao, N.-Z., Liu, S.-J. (2006). Yangia pacifica gen. nov., sp. nov., a novel member of the Roseobacter clade from coastal sediment of the East China Sea.. Int. J. Syst. Evol. Microbiol. 56: 529-533 [Abstract] [Full Text]  
  • Janssen, P. H. (2006). Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes.. Appl. Environ. Microbiol. 72: 1719-1728 [Full Text]  
  • Alonso, C., Pernthaler, J. (2006). Concentration-dependent patterns of leucine incorporation by coastal picoplankton.. Appl. Environ. Microbiol. 72: 2141-2147 [Abstract] [Full Text]  
  • Langenheder, S., Lindstrom, E. S., Tranvik, L. J. (2006). Structure and Function of Bacterial Communities Emerging from Different Sources under Identical Conditions. Appl. Environ. Microbiol. 72: 212-220 [Abstract] [Full Text]  
  • Longnecker, K., Sherr, B. F., Sherr, E. B. (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 [Abstract] [Full Text]  
  • Lozupone, C., Knight, R. (2005). UniFrac: a New Phylogenetic Method for Comparing Microbial Communities. Appl. Environ. Microbiol. 71: 8228-8235 [Abstract] [Full Text]  
  • Buchan, A., Gonzalez, J. M., Moran, M. A. (2005). Overview of the Marine Roseobacter Lineage. Appl. Environ. Microbiol. 71: 5665-5677 [Full Text]  
  • Comeau, A. M., Buenaventura, E., Suttle, C. A. (2005). A Persistent, Productive, and Seasonally Dynamic Vibriophage Population within Pacific Oysters (Crassostrea gigas). Appl. Environ. Microbiol. 71: 5324-5331 [Abstract] [Full Text]  
  • Pernthaler, J., Amann, R. (2005). Fate of Heterotrophic Microbes in Pelagic Habitats: Focus on Populations. Microbiol. Mol. Biol. Rev. 69: 440-461 [Abstract] [Full Text]  
  • Pernthaler, A., Pernthaler, J. (2005). Diurnal Variation of Cell Proliferation in Three Bacterial Taxa from Coastal North Sea Waters. Appl. Environ. Microbiol. 71: 4638-4644 [Abstract] [Full Text]  
  • Simu, K., Holmfeldt, K., Zweifel, U. L., Hagstrom, A. (2005). Culturability and Coexistence of Colony-Forming and Single-Cell Marine Bacterioplankton. Appl. Environ. Microbiol. 71: 4793-4800 [Abstract] [Full Text]  
  • Jasti, S., Sieracki, M. E., Poulton, N. J., Giewat, M. W., Rooney-Varga, J. N. (2005). Phylogenetic Diversity and Specificity of Bacteria Closely Associated with Alexandrium spp. and Other Phytoplankton. Appl. Environ. Microbiol. 71: 3483-3494 [Abstract] [Full Text]  
  • Floyd, M. M., Tang, J., Kane, M., Emerson, D. (2005). Captured Diversity in a Culture Collection: Case Study of the Geographic and Habitat Distributions of Environmental Isolates Held at the American Type Culture Collection. Appl. Environ. Microbiol. 71: 2813-2823 [Full Text]  
  • Alonso, C., Pernthaler, J. (2005). Incorporation of Glucose under Anoxic Conditions by Bacterioplankton from Coastal North Sea Surface Waters. Appl. Environ. Microbiol. 71: 1709-1716 [Abstract] [Full Text]  
  • Thompson, F. L., Iida, T., Swings, J. (2004). Biodiversity of Vibrios. Microbiol. Mol. Biol. Rev. 68: 403-431 [Abstract] [Full Text]  
  • Zhou, X., Bent, S. J., Schneider, M. G., Davis, C. C., Islam, M. R., Forney, L. J. (2004). Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology 150: 2565-2573 [Abstract] [Full Text]  
  • Thompson, J. R., Randa, M. A., Marcelino, L. A., Tomita-Mitchell, A., Lim, E., Polz, M. F. (2004). Diversity and Dynamics of a North Atlantic Coastal Vibrio Community. Appl. Environ. Microbiol. 70: 4103-4110 [Abstract] [Full Text]  
  • Cho, J.-C., Giovannoni, S. J. (2004). Robiginitalea biformata gen. nov., sp. nov., a novel marine bacterium in the family Flavobacteriaceae with a higher G+C content. Int. J. Syst. Evol. Microbiol. 54: 1101-1106 [Abstract] [Full Text]  
  • Skovhus, T. L., Ramsing, N. B., Holmstrom, C., Kjelleberg, S., Dahllof, I. (2004). Real-Time Quantitative PCR for Assessment of Abundance of Pseudoalteromonas Species in Marine Samples. Appl. Environ. Microbiol. 70: 2373-2382 [Abstract] [Full Text]  
  • Sunamura, M., Higashi, Y., Miyako, C., Ishibashi, J.-i., Maruyama, A. (2004). Two Bacteria Phylotypes Are Predominant in the Suiyo Seamount Hydrothermal Plume. Appl. Environ. Microbiol. 70: 1190-1198 [Abstract] [Full Text]  
  • Cho, J.-C., Giovannoni, S. J. (2004). Cultivation and Growth Characteristics of a Diverse Group of Oligotrophic Marine Gammaproteobacteria. Appl. Environ. Microbiol. 70: 432-440 [Abstract] [Full Text]  
  • Burkert, U., Warnecke, F., Babenzien, D., Zwirnmann, E., Pernthaler, J. (2003). Members of a Readily Enriched {beta}-Proteobacterial Clade Are Common in Surface Waters of a Humic Lake. Appl. Environ. Microbiol. 69: 6550-6559 [Abstract] [Full Text]  
  • Adachi, M., Kanno, T., Okamoto, R., Itakura, S., Yamaguchi, M., Nishijima, T. (2003). Population Structure of Alexandrium (Dinophyceae) Cyst Formation-Promoting Bacteria in Hiroshima Bay, Japan. Appl. Environ. Microbiol. 69: 6560-6568 [Abstract] [Full Text]  
  • Kirchman, D. L., Yu, L., Cottrell, M. T. (2003). Diversity and Abundance of Uncultured Cytophaga-Like Bacteria in the Delaware Estuary. Appl. Environ. Microbiol. 69: 6587-6596 [Abstract] [Full Text]  
  • Brinkmeyer, R., Knittel, K., Jurgens, J., Weyland, H., Amann, R., Helmke, E. (2003). Diversity and Structure of Bacterial Communities in Arctic versus Antarctic Pack Ice. Appl. Environ. Microbiol. 69: 6610-6619 [Abstract] [Full Text]  
  • Biegala, I. C., Not, F., Vaulot, D., Simon, N. (2003). Quantitative Assessment of Picoeukaryotes in the Natural Environment by Using Taxon-Specific Oligonucleotide Probes in Association with Tyramide Signal Amplification-Fluorescence In Situ Hybridization and Flow Cytometry. Appl. Environ. Microbiol. 69: 5519-5529 [Abstract] [Full Text]  
  • Martin, S., Marquez, M. C., Sanchez-Porro, C., Mellado, E., Arahal, D. R., Ventosa, A. (2003). Marinobacter lipolyticus sp. nov., a novel moderate halophile with lipolytic activity. Int. J. Syst. Evol. Microbiol. 53: 1383-1387 [Abstract] [Full Text]  
  • Sebat, J. L., Colwell, F. S., Crawford, R. L. (2003). Metagenomic Profiling: Microarray Analysis of an Environmental Genomic Library. Appl. Environ. Microbiol. 69: 4927-4934 [Abstract] [Full Text]  
  • Kisand, V., Wikner, J. (2003). Combining Culture-Dependent and -Independent Methodologies for Estimation of Richness of Estuarine Bacterioplankton Consuming Riverine Dissolved Organic Matter. Appl. Environ. Microbiol. 69: 3607-3616 [Abstract] [Full Text]  
  • Wagner-Dobler, I., Rheims, H., Felske, A., Pukall, R., Tindall, B. J. (2003). Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea. Int. J. Syst. Evol. Microbiol. 53: 731-738 [Abstract] [Full Text]  
  • Beardsley, C., Pernthaler, J., Wosniok, W., Amann, R. (2003). Are Readily Culturable Bacteria in Coastal North Sea Waters Suppressed by Selective Grazing Mortality?. Appl. Environ. Microbiol. 69: 2624-2630 [Abstract] [Full Text]  
  • Pernthaler, J., Pernthaler, A., Amann, R. (2003). Automated Enumeration of Groups of Marine Picoplankton after Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 69: 2631-2637 [Abstract] [Full Text]  
  • Sekar, R., Pernthaler, A., Pernthaler, J., Warnecke, F., Posch, T., Amann, R. (2003). An Improved Protocol for Quantification of Freshwater Actinobacteria by Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 69: 2928-2935 [Abstract] [Full Text]  
  • Tamaki, H., Hanada, S., Kamagata, Y., Nakamura, K., Nomura, N., Nakano, K., Matsumura, M. (2003). Flavobacterium limicola sp. nov., a psychrophilic, organic-polymer-degrading bacterium isolated from freshwater sediments. Int. J. Syst. Evol. Microbiol. 53: 519-526 [Abstract] [Full Text]  
  • Peplies, J., Glockner, F. O., Amann, R. (2003). Optimization Strategies for DNA Microarray-Based Detection of Bacteria with 16S rRNA-Targeting Oligonucleotide Probes. Appl. Environ. Microbiol. 69: 1397-1407 [Abstract] [Full Text]  
  • Fernandez-Martinez, J., Pujalte, M. J., Garcia-Martinez, J., Mata, M., Garay, E., Rodriguez-Valera, F. (2003). Description of Alcanivorax venustensis sp. nov. and reclassification of Fundibacter jadensis DSM 12178T (Bruns and Berthe-Corti 1999) as Alcanivorax jadensis comb. nov., members of the emended genus Alcanivorax. Int. J. Syst. Evol. Microbiol. 53: 331-338 [Abstract] [Full Text]  
  • Zengler, K., Toledo, G., Rappe, M., Elkins, J., Mathur, E. J., Short, J. M., Keller, M. (2002). Cultivating the uncultured. Proc. Natl. Acad. Sci. USA 99: 15681-15686 [Abstract] [Full Text]  
  • Pernthaler, A., Pernthaler, J., Schattenhofer, M., Amann, R. (2002). Identification of DNA-Synthesizing Bacterial Cells in Coastal North Sea Plankton. Appl. Environ. Microbiol. 68: 5728-5736 [Abstract] [Full Text]  
  • Bruns, A., Cypionka, H., Overmann, J. (2002). Cyclic AMP and Acyl Homoserine Lactones Increase the Cultivation Efficiency of Heterotrophic Bacteria from the Central Baltic Sea. Appl. Environ. Microbiol. 68: 3978-3987 [Abstract] [Full Text]  
  • Pernthaler, A., Pernthaler, J., Amann, R. (2002). Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria. Appl. Environ. Microbiol. 68: 3094-3101 [Abstract] [Full Text]  
  • Iwabuchi, N., Sunairi, M., Urai, M., Itoh, C., Anzai, H., Nakajima, M., Harayama, S. (2002). Extracellular Polysaccharides of Rhodococcus rhodochrous S-2 Stimulate the Degradation of Aromatic Components in Crude Oil by Indigenous Marine Bacteria. Appl. Environ. Microbiol. 68: 2337-2343 [Abstract] [Full Text]  
  • Bano, N., Hollibaugh, J. T. (2002). Phylogenetic Composition of Bacterioplankton Assemblages from the Arctic Ocean. Appl. Environ. Microbiol. 68: 505-518 [Abstract] [Full Text]  
  • Pernthaler, A., Preston, C. M., Pernthaler, J., DeLong, E. F., Amann, R. (2002). Comparison of Fluorescently Labeled Oligonucleotide and Polynucleotide Probes for the Detection of Pelagic Marine Bacteria and Archaea. Appl. Environ. Microbiol. 68: 661-667 [Abstract] [Full Text]  
  • Wirsen, C. O., Sievert, S. M., Cavanaugh, C. M., Molyneaux, S. J., Ahmad, A., Taylor, L. T., DeLong, E. F., Taylor, C. D. (2002). Characterization of an Autotrophic Sulfide-Oxidizing Marine Arcobacter sp. That Produces Filamentous Sulfur. Appl. Environ. Microbiol. 68: 316-325 [Abstract] [Full Text]  
  • Kisand, V., Cuadros, R., Wikner, J. (2002). Phylogeny of Culturable Estuarine Bacteria Catabolizing Riverine Organic Matter in the Northern Baltic Sea. Appl. Environ. Microbiol. 68: 379-388 [Abstract] [Full Text]  
  • Sass, A. M., Sass, H., Coolen, M. J. L., Cypionka, H., Overmann, J. (2001). Microbial Communities in the Chemocline of a Hypersaline Deep-Sea Basin (Urania Basin, Mediterranean Sea). Appl. Environ. Microbiol. 67: 5392-5402 [Abstract] [Full Text]  
  • Eguchi, M., Ostrowski, M., Fegatella, F., Bowman, J., Nichols, D., Nishino, T., Cavicchioli, R. (2001). Sphingomonas alaskensis Strain AFO1, an Abundant Oligotrophic Ultramicrobacterium from the North Pacific. Appl. Environ. Microbiol. 67: 4945-4954 [Abstract] [Full Text]  
  • Eilers, H., Pernthaler, J., Peplies, J., Glockner, F. O., Gerdts, G., Amann, R. (2001). Isolation of Novel Pelagic Bacteria from the German Bight and Their Seasonal Contributions to Surface Picoplankton. Appl. Environ. Microbiol. 67: 5134-5142 [Abstract] [Full Text]  
  • Pernthaler, A., Pernthaler, J., Eilers, H., Amann, R. (2001). Growth Patterns of Two Marine Isolates: Adaptations to Substrate Patchiness?. Appl. Environ. Microbiol. 67: 4077-4083 [Abstract] [Full Text]  
  • Pernthaler, J., Posch, T., Simek, K., Vrba, J., Pernthaler, A., Glöckner, F. O., Nübel, U., Psenner, R., Amann, R. (2001). Predator-Specific Enrichment of Actinobacteria from a Cosmopolitan Freshwater Clade in Mixed Continuous Culture. Appl. Environ. Microbiol. 67: 2145-2155 [Abstract] [Full Text]  
  • Ravenschlag, K., Sahm, K., Amann, R. (2001). Quantitative Molecular Analysis of the Microbial Community in Marine Arctic Sediments (Svalbard). Appl. Environ. Microbiol. 67: 387-395 [Abstract] [Full Text]  
  • Cottrell, M. T., Kirchman, D. L. (2000). Community Composition of Marine Bacterioplankton Determined by 16S rRNA Gene Clone Libraries and Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 66: 5116-5122 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Béjà, O., Aravind, L., Koonin, E. V., Suzuki, M. T., Hadd, A., Nguyen, L. P., Jovanovich, S. B., Gates, C. M., Feldman, R. A., Spudich, J. L., Spudich, E. N., DeLong, E. F. (2000). Bacterial Rhodopsin: Evidence for a New Type of Phototrophy in the Sea. Science 289: 1902-1906 [Abstract] [Full Text]