This Article
Right arrow Abstract Freely available
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 Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.
Agricola
Right arrow Articles by Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, April 2000, p. 1692-1697, Vol. 66, No. 4
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Natural Assemblages of Marine Proteobacteria and Members of the Cytophaga-Flavobacter Cluster Consuming Low- and High-Molecular-Weight Dissolved Organic Matter

Matthew T. Cottrell and David L. Kirchman*

College of Marine Studies, University of Delaware, Lewes, Delaware 19958

Received 23 September 1999/Accepted 12 January 2000


    ABSTRACT
Top
Abstract
Text
References

We used a method that combines microautoradiography with hybridization of fluorescent rRNA-targeted oligonucleotide probes to whole cells (MICRO-FISH) to test the hypothesis that the relative contributions of various phylogenetic groups to the utilization of dissolved organic matter (DOM) depend solely on their relative abundance in the bacterial community. We found that utilization of even simple low-molecular-weight DOM components by bacteria differed across the major phylogenetic groups and often did not correlate with the relative abundance of these bacterial groups in estuarine and coastal environments. The Cytophaga-Flavobacter cluster was overrepresented in the portion of the assemblage consuming chitin, N-acetylglucosamine, and protein but was generally underrepresented in the assemblage consuming amino acids. The amino acid-consuming assemblage was usually dominated by the alpha  subclass of the class Proteobacteria, although the representation of alpha -proteobacteria in the protein-consuming assemblages was about that expected from their relative abundance in the entire bacterial community. In our experiments, no phylogenetic group dominated the consumption of all DOM, suggesting that the participation of a diverse assemblage of bacteria is essential for the complete degradation of complex DOM in the oceans. These results also suggest that the role of aerobic heterotrophic bacteria in carbon cycling would be more accurately described by using three groups instead of the single bacterial compartment currently used in biogeochemical models.


    TEXT
Top
Abstract
Text
References

Analysis of 16S rRNA gene sequences (15) has greatly advanced our understanding of the phylogenetic diversity of bacteria and archaea (18), especially that of the vast majority of microbes in nature that have resisted cultivation to date (2). There is little information, however, on the metabolic function of specific bacterial groups in natural assemblages since few culture-independent studies have linked bacterial community structure and function (6). Although information on phylogenetic relationships of uncultured bacteria is readily accessible (14), the inability to culture most microbes limits the opportunities to assess their metabolic diversity. Even if appropriate culture conditions were to be found for the bulk of marine microbes, bacterial metabolism in the sea would probably remain poorly described, since metabolic behavior in culture is likely different from that in situ.

Extensive biogeochemical studies have shown that uptake and mineralization of dissolved organic matter (DOM) by bacteria constitute a major component of carbon cycling in aquatic ecosystems (11). Although the importance of DOM uptake is well recognized, the relative contributions of the major phylogenetic groups of bacteria to DOM uptake in the oceans are unknown (29). Differences in usage of various DOM components may help explain the distribution of the major bacterial groups among soil, freshwater, and marine ecosystems (18). It may also be important to know the minimum number of bacterial phylogenetic groups necessary to describe and explain DOM uptake in order to improve models of carbon cycling in aquatic habitats. Currently these models implicitly assume that all heterotrophic bacteria are the same and consist of a single phylogenetic type (12).

The goal of this study was to determine whether the relative contributions of various phylogenetic groups to the utilization of DOM depend solely on their relative abundance in the bacterial community. We used a novel approach, combining microautoradiography and fluorescence in situ hybridization (MICRO-FISH) (22, 28) to determine DOM uptake by the bacterial divisions and subclasses typically comprising marine assemblages (16). Since the chemical composition and degradation of DOM differ as a function of molecular weight (3, 4), different groups of bacteria may be responsible for mineralizing low- and high-molecular-weight DOM. We hypothesized that all heterotrophic bacteria use low-molecular-weight DOM, specifically monomers that can be transported easily across cell membranes. High-molecular-weight DOM, on the other hand, may be consumed by a smaller, less-diverse group of bacteria since specific extracellular enzymes are required for the hydrolysis of biopolymers, a component of high-molecular-weight DOM. To test these hypotheses, we used MICRO-FISH to compare utilization of protein and chitin by various phylogenetic groups with their utilization of amino acids and N-acetylglucosamine (NAG). Protein and chitin were chosen because they represent potentially large components of high-molecular-weight DOM (25).

Sample collection and incubation. Seawater was collected from the Delaware Bay estuary at the Roosevelt Inlet (salinity [S] = 30 ppt, temperature [T] = 14°C) and from the Atlantic Ocean at the Indian River Inlet (S = 32 ppt, T = 12°C) in November and December, respectively. Aliquots were incubated at 12 to 19°C and tritiated amino acids, NAG, protein, and chitin were added. The final concentrations of the amino acid mixture (47 Ci/mmol; Amersham) and NAG (9.9 Ci/mmol; Amersham) additions were 2.1 and 10 nM, respectively. Soluble chitin oligomers were prepared by mild acid hydrolysis (3 N HCl, 70°C, 5 min) of tritiated chitin purified from the marine fungus Paeosphaeria spartinicola (27) grown on medium containing [3H]NAG (21). Tritiated protein was prepared from Vibrio alginolyticus grown on medium containing [3H]leucine (26). Subsamples were filtered through 0.2-µm-pore-size polycarbonate filters to measure the uptake of radiolabeled compounds in incubations lasting 1 to 26 h. Amino acid incubations were for 1 h, the protein incubation with the assemblage from Roosevelt Inlet lasted 26 h, and the remaining incubations were for 7 h. Bacterial abundance was measured by determining 4',6'-diamidino-2-phenylindole (DAPI) direct counts (30).

MICRO-FISH. Samples were prepared for MICRO-FISH by using a variation of methods combining microautoradiography and fluorescence in situ hybridization. Unlike substrate-tracking autoradiographic fluorescent in situ hybridization (28), but similar to the protocol of Lee et al. (22), cells were transferred to glass coverslips and probed with fluorescent oligonucleotides before being coated with an autoradiographic film emulsion. After incubation with tritiated compounds, samples were fixed with formaldehyde, subsamples for MICRO-FISH were filtered through 0.2-µm-pore-size polycarbonate filters, and the cells were transferred to glass coverslips freshly treated with a 2% solution of 3-aminopropyltriethoxysilane (Sigma) (5). Immediately after filtration, the polycarbonate filter was placed face down on a coverslip, clamped together between two glass slides by the use of a large paper clip, and incubated for 1 h at 42°C. The filter was then peeled away, and the cells were dehydrated by passing the coverslip through a series of ethanol rinses and then air dried. Unlike the protocol of Lee et al. (22), our method does not require a special slide with a hole for viewing cells attached to the back of the coverslip.

In situ hybridization was done by placing the cell-adherent side of the coverslip in contact with a 30-µl drop of hybridization solution containing 2 ng of probe/µl in the bottom of a polystyrene petri dish. The probes used were as follows: for bacteria, Eub338 (positive control) (1); for alpha -proteobacteria, Alf1b (24); for beta -proteobacteria, Bet42a (24); for gamma -proteobacteria, Gam42a (24); for the Cytophaga-Flavobacter cluster of the Cytophaga-Flavobacter-Bacteroides division, CF319a (23); and for gram-positive bacteria with high DNA G+C content, HGC69a (32). The dish was sealed with Parafilm and incubated at 42°C for 2 h, after which the coverslip was incubated for 30 min at 48°C in a wash solution containing NaCl at a concentration appropriate for the probe (34). The coverslip was then rinsed in deionized water, air dried, and mounted (by the use of immersion oil) on a glass slide with the cell-adherent side of the coverslip facing away from the slide.

Samples were prepared for microautoradiography by dipping the glass slide, with coverslip attached, into a molten (43°C) NBT-2 emulsion (Kodak) diluted to 2 parts emulsion and 1 part deionized water. After incubation at -20°C for 2 days, the slides were warmed to room temperature and the photographic emulsion was developed by using Dektol developer (Kodak), a deionized-water stop bath, and fixer (Kodak) in accordance with the manufacturer's instructions. The slide was stained in a 2-µg/ml solution of DAPI for 2 min, dipped in deionized water, and air dried. The coverslip was removed from the glass slide and mounted on a clean glass slide with the cells facing the slide, using Citifluor (Ted Pella Inc., Redding, Calif.). Cells were examined by using a fluorescence microscope fitted with filter sets for DAPI (UV1A; Nikon) and Cy3 (41007A; Chroma). The average level of retention of cells on the coverslip through all steps of the procedure was 103%, as determined by DAPI counts of bacteria on black polycarbonate filters (30).

Phylogenetic groups consuming DOM compounds. MICRO-FISH identifies bacteria that have taken up tritiated compounds by determining the presence of silver grains adjacent to cells (Fig. 1). The phylogenetic classification of cells is determined by the binding of rRNA-targeted oligonucleotide probes conjugated to the yellow-fluorescing fluorochrome Cy3 (Fig. 1B). The sample shown in Fig. 1 was prepared by using tritiated amino acids typically consumed by a large fraction of cells (10, 19) and a positive-control probe complementary to a region of the 16S rRNA conserved in most bacteria (Eub338) (1), so all bacteria consuming free amino acids and having sufficient numbers of ribosomes are visible. The eubacterial probe detected on average 80% (standard deviation, 9.0) of the bacterial abundance determined by DAPI direct counts.


View larger version (131K):
[in this window]
[in a new window]
 
FIG. 1.   Micrograph of bacteria assayed by MICRO-FISH. (A) DAPI-stained bacteria (UV excitation). Dark spots surrounding cells are silver grains deposited in photographic emulsion around cells that took up a mixture of tritiated free amino acids. Less than 0.6% of cells in formaldehyde-killed controls had silver grains. (B) Bacteria hybridized with Cy3-labeled oligonucleotide probe Eub338 for eubacteria (green excitation). Cells with bound probe fluoresce yellow. Magnification, ×1,350.

Bacterial assemblages in Delaware estuarine and coastal waters were dominated by proteobacteria and members of the Cytophaga-Flavobacter cluster (Fig. 2A and 3A). Proteobacteria, and to a lesser extent the Cytophaga-Flavobacter cluster, are typically abundant in aquatic systems (31, 33). Three subclasses of proteobacteria (alpha , beta , and gamma ) were about equally abundant in the coastal sample, while alpha -proteobacteria were most abundant in the estuarine sample. The relatively large abundance of members of the Cytophaga-Flavobacter cluster may be a consequence of high particle loads in these environments; studies inferring community composition from libraries of cloned 16S rRNA genes amplified by PCR have found that this group is enriched on particles (9). However, Glöckner et al. (16), using fluorescence in situ hybridization, found that a large abundance of bacteria in the Cytophaga-Flavobacter cluster may be common in marine systems. Cells binding the probe for gram-positive bacteria accounted for less than 3% of the direct count, which is not significantly different from counts of autofluorescent cells in controls without a probe. The probes for alpha -, beta -, and gamma -proteobacteria and the Cytophaga-Flavobacter cluster detected 70% (standard deviation, 30) of the bacteria visualized with the control probe (Eub338) for all bacteria (Fig. 2A and 3A).


View larger version (44K):
[in this window]
[in a new window]
 
FIG. 2.   Community composition and consumption of chitin, NAG, protein, and amino acids by the major phylogenetic groups of bacterioplankton in the Roosevelt Inlet, assayed by MICRO-FISH. (A) Composition of bacterioplankton communities in incubations containing tritiated compounds. (B) Relative abundance of phylogenetic groups of bacteria consuming various tritiated compounds. Less than 3% of the cells were gram positive. Cells binding none of the group-specific probes are indicated (Not identified). Percentages were calculated relative to total bacteria counted by using DAPI, although the eubacterial probe (Eub338) detected on average 80% of bacterial abundance. proteobact., proteobacteria; Flavobact., Flavobacter.


View larger version (43K):
[in this window]
[in a new window]
 
FIG. 3.   Community composition and consumption of chitin, NAG, protein, and amino acids by the major phylogenetic groups of bacterioplankton in the Indian River Inlet, assayed by MICRO-FISH. (A) Composition of bacterioplankton communities in incubations containing tritiated compounds. (B) Relative abundance of phylogenetic groups of bacteria consuming various tritiated compounds. Less than 3% of the cells were gram positive. Cells binding none of the group-specific probes are indicated (Not identified). Percentages were calculated relative to total bacteria counted by using DAPI, although the eubacterial probe (Eub338) detected on average 80% of the bacterial abundance.

Consumption of organic compounds differed among the phylogenetic groups. Even uptake of low-molecular-weight DOM differed greatly among groups. The Cytophaga-Flavobacter cluster accounted for the largest fraction of bacteria consuming chitin, NAG, and protein but was the smallest fraction consuming amino acids (Fig. 2B and Fig. 3B). In contrast, alpha -proteobacteria comprised the largest fraction of the community consuming amino acids but the smallest fraction consuming protein. Differences between amino acid consumption by alpha -proteobacteria and by members of the Cytophaga-Flavobacter cluster occurred in both estuarine and coastal environments (Fig. 2B and 3B), but consumption of amino acids by these two groups in the San Pedro Channel off the California coast did not differ (28). In the San Pedro Channel, these two groups were equally abundant and about 80% of the cells in each group actively took up amino acids.

Although a large (>50%) fraction of bacteria sometimes could not be identified with the four group-specific probes used in this study (Fig. 2A and 3A), usually only a small fraction (<20%) of the bacteria actively taking up the various 3H-labeled compounds remained unidentified (Fig. 2B and 3B). The single exception occurred in the estuarine experiment examining chitin utilization. Nearly 40% of the bacteria assimilating 3H-chitin oligomers could not be assigned to one of the four phylogenetic groups examined (Fig. 2B).

There was no fixed relationship between utilization of polymers and their constituent monomers by different phylogenetic groups. The same phylogenetic groups accounted for most of the cells consuming chitin and NAG, but protein and amino acids were largely consumed by different phylogenetic groups. Members of the Cytophaga-Flavobacter cluster accounted for 30 and 47% of the community consuming chitin and NAG, respectively, and alpha -proteobacteria accounted for 22 and 45% of the cells consuming these compounds, respectively. In contrast, the Cytophaga-Flavobacter cluster accounted for 45% of the cells consuming protein but only 3% of the cells consuming amino acids, while alpha -proteobacteria accounted for 45% of the cells consuming amino acids but only 10% of the cells consuming protein.

Composition and activity of bacterial assemblages. The distributions of beta - and gamma -proteobacteria are among the most striking features of microbial diversity in aquatic environments. Although these two groups coexist in coastal environments (31), beta -proteobacteria are not found in the oligotrophic ocean but are abundant in freshwater habitats, where they seem to displace gamma -proteobacteria (16, 17). Variations in the supply and composition of DOM in freshwater versus marine systems (3, 13) may determine the distribution of beta - and gamma -proteobacteria if these two groups differ in the capacity to utilize various DOM components. Our hypothesis is based on the observation that growth of the total bacterial community is often limited by the availability of DOM (7, 8, 20). An alternative hypothesis is that beta - and gamma -proteobacteria use the same compounds present in both oceanic and freshwater environments and that beta -proteobacteria are restricted from the oligotrophic ocean by a selection factor other than DOM.

Our results suggest that beta - and gamma -proteobacteria are similar with respect to DOM consumption. These two groups comprised the smallest fraction (15% or less) of bacteria consuming chitin and NAG, and they accounted for 19 to 29% of the cells consuming protein and amino acids. This analysis suggests that the availability of DOM does not explain the distributions of beta - and gamma -proteobacteria in aquatic environments.

The relative abundance of phylogenetic groups of bacteria in assemblages consuming various DOM components often differed from their relative abundance in the assemblage as a whole. The Cytophaga-Flavobacter cluster was overrepresented in the portion of the assemblage consuming chitin (Fig. 4A), NAG (Fig. 4B), and protein (Fig. 4C). Among the cells identified by the bacterial probe (Eub338), the Cytophaga-Flavobacter cluster comprised 23 to 55% of the cells consuming chitin, NAG, and protein, but these bacteria made up only 8 to 38% of the assemblage (Fig. 4A to C). In contrast, the Cytophaga-Flavobacter cluster was greatly underrepresented in the assemblage consuming amino acids (Fig. 4D), accounting for only 2 to 4% of the amino acid-consuming bacteria. All three subclasses of proteobacteria were equally or underrepresented among bacteria consuming chitin (Fig. 4A), but their participation in protein usage was less clear. Protein use by alpha -proteobacteria was about that expected from their relative abundance in the total bacterial community, while beta - and gamma -proteobacteria were over and underrepresented among the bacteria consuming protein in the two environments sampled in this study (Fig. 4C). The beta  and gamma  subclasses of proteobacteria comprised a small portion of the assemblage (<10%) consuming NAG relative to their abundance (10 to 25%) (Fig. 4B). Uptake of amino acids differed greatly among the three subclasses of proteobacteria and between experiments. The percentage of amino acid-consuming bacteria that were proteobacteria sometimes was greater than, equal to, and less than their contribution to total bacterial abundance (Fig. 4D).


View larger version (30K):
[in this window]
[in a new window]
 
FIG. 4.   Relationship among the phylogenetic classifications of bacteria consuming chitin (A), NAG (B), protein (C), and amino acids (D) versus phylogenetic classification of cells identified as eubacteria. Bacteria were classified by using rRNA-binding oligonucleotide probes specific for alpha -proteobacteria (alpha ), beta -proteobacteria (beta ), gamma -proteobacteria (gamma ), and the Cytophaga-Flavobacter group (C). Data points falling above the 1:1 line indicate phylogenetic groups enriched in the portion of the assemblage consuming the compound. Results are from coastal (Fig. 2) and estuarine (Fig. 3) environments. Percentages were calculated relative to the numbers of cells identified as eubacteria with the Eub338 probe.

Changes in community structure due to protein addition were consistent with the MICRO-FISH results. Addition of protein in the Roosevelt Inlet experiment caused a large increase in the abundance of the same bacterial groups revealed by MICRO-FISH to consume protein. alpha -Proteobacteria initially dominated the community (27% of the total), but after incubation with protein, bacteria in the Cytophaga-Flavobacter cluster were the most abundant (35% of the community) and alpha -proteobacteria were the least abundant (Fig. 2A). MICRO-FISH indicated that 45% of the cells consuming protein were members of the Cytophaga-Flavobacter cluster and that only 2% were alpha -proteobacteria (Fig. 2B). Cytophaga-Flavobacter cluster members did not dominate protein consumption simply because they grow rapidly in bottle incubations while alpha -proteobacteria grow slowly. In a shorter incubation with an assemblage from the Indian River Inlet, there was no shift in the community composition (Fig. 3A). MICRO-FISH again revealed that members of the Cytophaga-Flavobacter cluster accounted for most of the cells consuming protein and that alpha -proteobacteria accounted for the smallest fraction (Fig. 3B).

In revealing the differences in DOM uptake by the various heterotrophic bacteria, this study indicates the need to consider more than a single compartment for modeling the role of heterotrophic bacteria in carbon cycles. However, our results also suggest that models may not require inclusion of the entire diverse spectrum of organisms found by culture-independent studies (15, 18). We found that, with one exception, all of the bacteria assimilating DOM components could be assigned to one of the four phylogenetic groups examined, although other bacterial groups undoubtedly assimilate some DOM. Furthermore, since beta -proteobacteria are not commonly found in oceans (16, 18), and in any case their activity seems similar to that of gamma -proteobacteria, it appears that uptake of DOM may be explained by three bacterial groups, with properties represented by alpha - and gamma -proteobacteria and the Cytophaga-Flavobacter cluster. Our generalization about DOM uptake, however, may not apply to other environments (e.g., soils), where these three phylogenetic groups probably have different metabolic capacities.

In general, the number of groups required to describe relationships between bacterial community structure and function is unclear. The phylogenetic level on which to focus is also not obvious. In our study, we found that consumption of DOM could be explained using a relatively small number of phylogenetic groups (at most four) at the division and subclass levels. Understanding other structure-function relationships, however, may require examining a larger number of more closely related phylogenetic groups. For example, temporal shifts in DOM consumption might be explained at the family or genus level, and more bacterial groups may be necessary for explaining DOM uptake in aquatic environments (e.g., oligotrophic oceans) that differ greatly from the eutrophic waters of our study. Although more data are clearly needed, our study suggests that comparing DOM consumption across environments at the division and proteobacterial-subclass levels will enhance our understanding of this structure-function relationship in marine bacterial communities.


    ACKNOWLEDGMENTS

This research was supported by the U.S. Department of Energy.


    FOOTNOTES

* Corresponding author. Mailing address: College of Marine Studies, University of Delaware, 700 Pilottown Rd., Lewes, DE 19958. Phone: (302) 645-4375. Fax: (302) 645-4028. E-mail: kirchman{at}udel.edu.


    REFERENCES
Top
Abstract
Text
References

1. Amann, R. I., B. J. Binder, R. J. Olson, S. W. Chisholm, R. Devereux, and D. A. Stahl. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925[Abstract/Free Full Text].
2. Amann, R. I., W. Ludwig, and K.-H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169[Abstract/Free Full Text].
3. Amon, R. M. W., and R. Benner. 1996. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 41:41-51.
4. Amon, R. M. W., and R. Benner. 1994. Rapid cycling of high-molecular-weight dissolved organic matter in the ocean. Nature 369:549-551[CrossRef].
5. Barer, M. R., and A. Entwistle. 1991. Confocal microscopy of surface labeled and cytoplasmically labeled bacteria immobilized by APS centrifugation. Lett. Appl. Microbiol. 13:186-189.
6. Boschker, H. T. S., S. C. Nold, P. Wellsbury, D. Bos, W. de Graaf, R. Pel, R. J. Parkes, and T. E. Cappenberg. 1998. Direct linking of microbial populations to specific biogeochemical processes by 13C labelling of biomarkers. Nature 392:801-805[CrossRef].
7. 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[CrossRef].
8. Chin-Leo, G., and R. Benner. 1992. Enhanced bacterioplankton production and respiration at intermediate salinities in the Mississippi River plume. Mar. Ecol. Prog. Ser. 87:87-103.
9. DeLong, E. F., D. G. Franks, and A. L. Alldredge. 1993. Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol. Oceanogr. 38:924-934.
10. Douglas, D. J., 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. 36:91-99[CrossRef].
11. Ducklow, H. W., and C. A. Carlson. 1992. Oceanic bacterial production. Adv. Microb. Ecol. 12:113-181.
12. Fasham, M. J. R., P. W. Boyd, and G. Savidge. 1999. Modeling the relative contributions of autotrophs and heterotrophs to carbon flow at a Lagrangian JGOFS station in the Northeast Atlantic: the importance of DOC. Limnol. Oceanogr. 44:80-94.
13. Findlay, S., R. L. Sinsabaugh, D. T. Fischer, and P. Franchini. 1998. Sources of dissolved organic carbon supporting planktonic bacterial production in the tidal freshwater Hudson River. Ecosystems 1:227-239[CrossRef].
14. Giovannoni, S., and S. C. Cary. 1993. Probing marine systems with ribosomal RNAs. Oceanography 6:95-104.
15. Giovannoni, S. J., T. B. Britschgi, C. L. Moyer, and K. G. Field. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60-63[CrossRef][Medline].
16. Glöckner, F. O., B. M. Fuchs, and R. Amann. 1999. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65:3721-3726[Abstract/Free Full Text].
17. Hiorns, W. D., B. A. Methé, S. A. Nierzwicki-Bauer, and J. P. Zehr. 1997. Bacterial diversity in Adirondack Mountain lakes as revealed by 16S rRNA gene sequences. Appl. Environ. Microbiol. 63:2957-2960[Abstract].
18. Hugenholtz, P., B. M. Goebel, and N. R. Pace. 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180:4765-4774[Free Full Text].
19. Karner, M., and J. A. Fuhrman. 1997. Determination of active marine bacterioplankton: a comparison of universal 16S rRNA probes, autoradiography, and nucleoid staining. Appl. Environ. Microbiol. 63:1208-1213[Abstract].
20. Kirchman, D. L., and J. H. Rich. 1997. Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb. Ecol. 33:11-20[CrossRef][Medline].
21. Kirchman, D. L., and J. White. 1999. Hydrolysis and mineralization of chitin in the Delaware Estuary. Aquat. Microb. Ecol. 18:187-196[CrossRef].
22. Lee, N., P. H. Nielsen, K. H. Andreasen, S. Juretschko, J. L. Nielsen, K.-H. Schleifer, and M. Wagner. 1999. Combination of fluorescent in situ hybridization and microautoradiography---a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65:1289-1297[Abstract/Free Full Text].
23. Manz, W., R. Amann, W. Ludwig, M. Vancanneyt, and K.-H. Schleifer. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology (Reading) 142:1097-1106[Abstract/Free Full Text].
24. Manz, W., R. Amann, W. Ludwig, M. Wagner, and K.-H. Schleifer. 1992. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15:593-600.
25. McCarthy, M., T. Pratum, J. Hedges, and R. Benner. 1997. Chemical composition of dissolved organic nitrogen in the ocean. Nature 390:150-154[CrossRef].
26. Nagata, T., R. Fukuda, I. Koike, K. Kogure, and D. L. Kirchman. 1998. Degradation by bacteria of membrane and soluble protein in seawater. Aquat. Microb. Ecol. 14:29-37.
27. Newell, S. Y. 1993. Decomposition of shoots of a salt-marsh grass, p. 301-326. In J. G. Jones (ed.), Advances in microbial ecology. Plenum Press, New York, N.Y.
28. 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. 65:1746-1752[Abstract/Free Full Text].
29. Pinhassi, J., F. Azam, J. Hemphala, R. A. Long, J. Martinez, U. L. Zweifel, and A. Hagstrom. 1999. Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat. Microb. Ecol. 17:13-26[CrossRef].
30. Porter, K., and Y. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25:943-948.
31. Rappé, M. S., P. F. Kemp, and S. J. Giovannoni. 1997. Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina. Limnol. Oceanogr. 42:811-826.
32. Roller, C., M. Wagner, R. Amann, W. Ludwig, and K. H. Schleifer. 1994. In situ probing of gram-positive bacteria with high DNA G+C content using 23S ribosomal-RNA-targeted oligonucleotides. Microbiology (Reading) 140:2849-2858[Abstract/Free Full Text].
33. Suzuki, M. T., M. S. Rappé, Z. W. Haimberger, H. Winfield, N. Adair, J. Ströbel, and S. J. Giovannoni. 1997. Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample. Appl. Environ. Microbiol. 63:983-989[Abstract].
34. Zarda, B., D. Hahn, A. Chatzinotas, W. Schonhuber, A. Neef, R. I. Amann, and J. Zeyer. 1997. Analysis of bacterial community structure in bulk soil by in situ hybridization. Arch. Microbiol. 168:185-192[CrossRef].


Applied and Environmental Microbiology, April 2000, p. 1692-1697, Vol. 66, No. 4
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • 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]  
  • Alonso-Saez, L., Unanue, M., Latatu, A., Azua, I., Ayo, B., Artolozaga, I., Iriberri, J. (2009). Changes in marine prokaryotic community induced by varying types of dissolved organic matter and subsequent grazing pressure. J PLANKTON RES 31: 1373-1383 [Abstract] [Full Text]  
  • Pinhassi, J., Nedashkovskaya, O. I., Hagstrom, A., Vancanneyt, M. (2009). Winogradskyella rapida sp. nov., isolated from protein-enriched seawater. Int. J. Syst. Evol. Microbiol. 59: 2180-2184 [Abstract] [Full Text]  
  • Park, S. C., Baik, K. S., Kim, M. S., Kim, S. S., Kim, S. R., Oh, M.-J., Kim, D., Bang, B.-H., Seong, C. N. (2009). Aequorivita capsosiphonis sp. nov., isolated from the green alga Capsosiphon fulvescens, and emended description of the genus Aequorivita. Int. J. Syst. Evol. Microbiol. 59: 724-728 [Abstract] [Full Text]  
  • Chauhan, A., Cherrier, J., Williams, H. N. (2009). Impact of sideways and bottom-up control factors on bacterial community succession over a tidal cycle. Proc. Natl. Acad. Sci. USA 106: 4301-4306 [Abstract] [Full Text]  
  • Zhao, M., Chen, F., Jiao, N. (2009). Genetic Diversity and Abundance of Flavobacterial Proteorhodopsin in China Seas. Appl. Environ. Microbiol. 75: 529-533 [Abstract] [Full Text]  
  • Grote, J., Jost, G., Labrenz, M., Herndl, G. J., Jurgens, K. (2008). Epsilonproteobacteria Represent the Major Portion of Chemoautotrophic Bacteria in Sulfidic Waters of Pelagic Redoxclines of the Baltic and Black Seas. Appl. Environ. Microbiol. 74: 7546-7551 [Abstract] [Full Text]  
  • Alain, K., Intertaglia, L., Catala, P., Lebaron, P. (2008). Eudoraea adriatica gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 58: 2275-2281 [Abstract] [Full Text]  
  • Khan, S. T., Nakagawa, Y., Harayama, S. (2008). Fulvibacter tottoriensis gen. nov., sp. nov., a member of the family Flavobacteriaceae isolated from marine sediment. Int. J. Syst. Evol. Microbiol. 58: 1670-1674 [Abstract] [Full Text]  
  • Gonzalez, J. M., Fernandez-Gomez, B., Fernandez-Guerra, A., Gomez-Consarnau, L., Sanchez, O., Coll-Llado, M., del Campo, J., Escudero, L., Rodriguez-Martinez, R., Alonso-Saez, L., Latasa, M., Paulsen, I., Nedashkovskaya, O., Lekunberri, I., Pinhassi, J., Pedros-Alio, C. (2008). From the Cover: Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc. Natl. Acad. Sci. USA 105: 8724-8729 [Abstract] [Full Text]  
  • Xia, Y., Kong, Y., Thomsen, T. R., Halkjaer Nielsen, P. (2008). Identification and Ecophysiological Characterization of Epiphytic Protein-Hydrolyzing Saprospiraceae ("Candidatus Epiflobacter" spp.) in Activated Sludge. Appl. Environ. Microbiol. 74: 2229-2238 [Abstract] [Full Text]  
  • Zubkov, M. V., Tarran, G. A., Mary, I., Fuchs, B. M. (2008). Differential microbial uptake of dissolved amino acids and amino sugars in surface waters of the Atlantic Ocean. J PLANKTON RES 30: 211-220 [Abstract] [Full Text]  
  • Haynes, K., Hofmann, T. A., Smith, C. J., Ball, A. S., Underwood, G. J. C., Osborn, A. M. (2007). Diatom-Derived Carbohydrates as Factors Affecting Bacterial Community Composition in Estuarine Sediments. Appl. Environ. Microbiol. 73: 6112-6124 [Abstract] [Full Text]  
  • Chen, S., Bagdasarian, M., Kaufman, M. G., Bates, A. K., Walker, E. D. (2007). Mutational Analysis of the ompA Promoter from Flavobacterium johnsoniae. J. Bacteriol. 189: 5108-5118 [Abstract] [Full Text]  
  • Woebken, D., Fuchs, B. M., Kuypers, M. M. M., Amann, R. (2007). Potential Interactions of Particle-Associated Anammox Bacteria with Bacterial and Archaeal Partners in the Namibian Upwelling System. Appl. Environ. Microbiol. 73: 4648-4657 [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]  
  • Eiler, A., Bertilsson, S. (2007). Flavobacteria Blooms in Four Eutrophic Lakes: Linking Population Dynamics of Freshwater Bacterioplankton to Resource Availability. Appl. Environ. Microbiol. 73: 3511-3518 [Abstract] [Full Text]  
  • Khan, S. T., Nakagawa, Y., Harayama, S. (2007). Galbibacter mesophilus gen. nov., sp. nov., a novel member of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 57: 969-973 [Abstract] [Full Text]  
  • Lennon, J. T. (2007). Diversity and Metabolism of Marine Bacteria Cultivated on Dissolved DNA. Appl. Environ. Microbiol. 73: 2799-2805 [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]  
  • Lau, W. W. Y., Keil, R. G., Armbrust, E. V. (2007). Succession and Diel Transcriptional Response of the Glycolate-Utilizing Component of the Bacterial Community during a Spring Phytoplankton Bloom. Appl. Environ. Microbiol. 73: 2440-2450 [Abstract] [Full Text]  
  • Rogers, S. W., Moorman, T. B., Ong, S. K. (2007). Fluorescent In Situ Hybridization and Micro-autoradiography Applied to Ecophysiology in Soil. Soil Sci. 71: 620-631 [Abstract] [Full Text]  
  • Chen, S., Bagdasarian, M., Kaufman, M. G., Walker, E. D. (2007). Characterization of Strong Promoters from an Environmental Flavobacterium hibernum Strain by Using a Green Fluorescent Protein-Based Reporter System. Appl. Environ. Microbiol. 73: 1089-1100 [Abstract] [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]  
  • Alonso-Saez, L., Gasol, J. M., Lefort, T., Hofer, J., Sommaruga, R. (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 [Abstract] [Full Text]  
  • Peterson, S. B., Dunn, A. K., Klimowicz, A. K., Handelsman, J. (2006). Peptidoglycan from Bacillus cereus Mediates Commensalism with Rhizosphere Bacteria from the Cytophaga-Flavobacterium Group. Appl. Environ. Microbiol. 72: 5421-5427 [Abstract] [Full Text]  
  • Pinhassi, J., Bowman, J. P., Nedashkovskaya, O. I., Lekunberri, I., Gomez-Consarnau, L., Pedros-Alio, C. (2006). Leeuwenhoekiella blandensis sp. nov., a genome-sequenced marine member of the family Flavobacteriaceae.. Int. J. Syst. Evol. Microbiol. 56: 1489-1493 [Abstract] [Full Text]  
  • Saha, P., Chakrabarti, T. (2006). Emticicia oligotrophica gen. nov., sp. nov., a new member of the family 'Flexibacteraceae', phylum Bacteroidetes.. Int. J. Syst. Evol. Microbiol. 56: 991-995 [Abstract] [Full Text]  
  • Lin, X., Wakeham, S. G., Putnam, I. F., Astor, Y. M., Scranton, M. I., Chistoserdov, A. Y., Taylor, G. T. (2006). Comparison of Vertical Distributions of Prokaryotic Assemblages in the Anoxic Cariaco Basin and Black Sea by Use of Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 72: 2679-2690 [Abstract] [Full Text]  
  • Ainsworth, T. D., Fine, M., Blackall, L. L., Hoegh-Guldberg, O. (2006). Fluorescence In Situ Hybridization and Spectral Imaging of Coral-Associated Bacterial Communities. Appl. Environ. Microbiol. 72: 3016-3020 [Abstract] [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]  
  • O'Sullivan, L. A., Rinna, J., Humphreys, G., Weightman, A. J., Fry, J. C. (2006). Culturable phylogenetic diversity of the phylum 'Bacteroidetes' from river epilithon and coastal water and description of novel members of the family Flavobacteriaceae: Epilithonimonas tenax gen. nov., sp. nov. and Persicivirga xylanidelens gen. nov., sp. nov.. Int. J. Syst. Evol. Microbiol. 56: 169-180 [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]  
  • Elifantz, H., Malmstrom, R. R., Cottrell, M. T., Kirchman, D. L. (2005). Assimilation of Polysaccharides and Glucose by Major Bacterial Groups in the Delaware Estuary. Appl. Environ. Microbiol. 71: 7799-7805 [Abstract] [Full Text]  
  • Kopke, B., Wilms, R., Engelen, B., Cypionka, H., Sass, H. (2005). Microbial Diversity in Coastal Subsurface Sediments: a Cultivation Approach Using Various Electron Acceptors and Substrate Gradients. Appl. Environ. Microbiol. 71: 7819-7830 [Abstract] [Full Text]  
  • Cottrell, M. T., Yu, L., Kirchman, D. L. (2005). Sequence and Expression Analyses of Cytophaga-Like Hydrolases in a Western Arctic Metagenomic Library and the Sargasso Sea. Appl. Environ. Microbiol. 71: 8506-8513 [Abstract] [Full Text]  
  • Yokokawa, T., Nagata, T. (2005). Growth and Grazing Mortality Rates of Phylogenetic Groups of Bacterioplankton in Coastal Marine Environments. Appl. Environ. Microbiol. 71: 6799-6807 [Abstract] [Full Text]  
  • Anderson, T. R. (2005). Plankton functional type modelling: running before we can walk?. J PLANKTON RES 27: 1073-1081 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Kenzaka, T., Ishidoshiro, A., Yamaguchi, N., Tani, K., Nasu, M. (2005). rRNA Sequence-Based Scanning Electron Microscopic Detection of Bacteria. Appl. Environ. Microbiol. 71: 5523-5531 [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]  
  • Okabe, S., Kindaichi, T., Ito, T. (2005). Fate of 14C-Labeled Microbial Products Derived from Nitrifying Bacteria in Autotrophic Nitrifying Biofilms. Appl. Environ. Microbiol. 71: 3987-3994 [Abstract] [Full Text]  
  • Malmstrom, R. R., Cottrell, M. T., Elifantz, H., Kirchman, D. L. (2005). Biomass Production and Assimilation of Dissolved Organic Matter by SAR11 Bacteria in the Northwest Atlantic Ocean. Appl. Environ. Microbiol. 71: 2979-2986 [Abstract] [Full Text]  
  • Aluwihare, L. I., Repeta, D. J., Pantoja, S., Johnson, C. G. (2005). Two Chemically Distinct Pools of Organic Nitrogen Accumulate in the Ocean. Science 308: 1007-1010 [Abstract] [Full Text]  
  • Olapade, O. A., Leff, L. G. (2005). Seasonal Response of Stream Biofilm Communities to Dissolved Organic Matter and Nutrient Enrichments. Appl. Environ. Microbiol. 71: 2278-2287 [Abstract] [Full Text]  
  • Lau, K. W. K., Ng, C. Y. M., Ren, J., Lau, S. C. L., Qian, P.-Y., Wong, P.-K., Lau, T. C., Wu, M. (2005). Owenweeksia hongkongensis gen. nov., sp. nov., a novel marine bacterium of the phylum 'Bacteroidetes'. Int. J. Syst. Evol. Microbiol. 55: 1051-1057 [Abstract] [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]  
  • Pinhassi, J., Sala, M. M., Havskum, H., Peters, F., Guadayol, OÒs., Malits, A., Marrase, C. (2004). Changes in Bacterioplankton Composition under Different Phytoplankton Regimens. Appl. Environ. Microbiol. 70: 6753-6766 [Abstract] [Full Text]  
  • Thompson, F. L., Iida, T., Swings, J. (2004). Biodiversity of Vibrios. Microbiol. Mol. Biol. Rev. 68: 403-431 [Abstract] [Full Text]  
  • Vila, M., Simo, R., Kiene, R. P., Pinhassi, J., Gonzalez, J. M., Moran, M. A., Pedros-Alio, C. (2004). Use of Microautoradiography Combined with Fluorescence In Situ Hybridization To Determine Dimethylsulfoniopropionate Incorporation by Marine Bacterioplankton Taxa. Appl. Environ. Microbiol. 70: 4648-4657 [Abstract] [Full Text]  
  • Malmstrom, R. R., Kiene, R. P., Cottrell, M. T., Kirchman, D. L. (2004). Contribution of SAR11 Bacteria to Dissolved Dimethylsulfoniopropionate and Amino Acid Uptake in the North Atlantic Ocean. Appl. Environ. Microbiol. 70: 4129-4135 [Abstract] [Full Text]  
  • Teira, E., Reinthaler, T., Pernthaler, A., Pernthaler, J., Herndl, G. J. (2004). Combining Catalyzed Reporter Deposition-Fluorescence In Situ Hybridization and Microautoradiography To Detect Substrate Utilization by Bacteria and Archaea in the Deep Ocean. Appl. Environ. Microbiol. 70: 4411-4414 [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]  
  • Lipson, D. A., Schmidt, S. K. (2004). Seasonal Changes in an Alpine Soil Bacterial Community in the Colorado Rocky Mountains. Appl. Environ. Microbiol. 70: 2867-2879 [Abstract] [Full Text]  
  • Kindaichi, T., Ito, T., Okabe, S. (2004). Ecophysiological Interaction between Nitrifying Bacteria and Heterotrophic Bacteria in Autotrophic Nitrifying Biofilms as Determined by Microautoradiography-Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 70: 1641-1650 [Abstract] [Full Text]  
  • Junge, K., Eicken, H., Deming, J. W. (2004). Bacterial Activity at -2 to -20{degrees}C in Arctic Wintertime Sea Ice. Appl. Environ. Microbiol. 70: 550-557 [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]  
  • Adamczyk, J., Hesselsoe, M., Iversen, N., Horn, M., Lehner, A., Nielsen, P. H., Schloter, M., Roslev, P., Wagner, M. (2003). The Isotope Array, a New Tool That Employs Substrate-Mediated Labeling of rRNA for Determination of Microbial Community Structure and Function. Appl. Environ. Microbiol. 69: 6875-6887 [Abstract] [Full Text]  
  • Bowman, J. P., Nichols, C. M., Gibson, J. A. E. (2003). Algoriphagus ratkowskyi gen. nov., sp. nov., Brumimicrobium glaciale gen. nov., sp. nov., Cryomorpha ignava gen. nov., sp. nov. and Crocinitomix catalasitica gen. nov., sp. nov., novel flavobacteria isolated from various polar habitats. Int. J. Syst. Evol. Microbiol. 53: 1343-1355 [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]  
  • Polz, M. F., Bertilsson, S., Acinas, S. G., Hunt, D. (2003). A(r)Ray of Hope in Analysis of the Function and Diversity of Microbial Communities. Biol. Bull. 204: 196-199 [Abstract] [Full Text]  
  • Riemann, L., Azam, F. (2002). Widespread N-Acetyl-D-Glucosamine Uptake among Pelagic Marine Bacteria and Its Ecological Implications. Appl. Environ. Microbiol. 68: 5554-5562 [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]  
  • Gattuso, J.-P., Peduzzi, S., Pizay, M.-D., Tonolla, M. (2002). Changes in freshwater bacterial community composition during measurements of microbial and community respiration. J PLANKTON RES 24: 1197-1206 [Abstract] [Full Text]  
  • Frias-Lopez, J., Zerkle, A. L., Bonheyo, G. T., Fouke, B. W. (2002). Partitioning of Bacterial Communities between Seawater and Healthy, Black Band Diseased, and Dead Coral Surfaces. Appl. Environ. Microbiol. 68: 2214-2228 [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]  
  • O'Sullivan, L. A., Weightman, A. J., Fry, J. C. (2002). New Degenerate Cytophaga-Flexibacter-Bacteroides-Specific 16S Ribosomal DNA-Targeted Oligonucleotide Probes Reveal High Bacterial Diversity in River Taff Epilithon. Appl. Environ. Microbiol. 68: 201-210 [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]  
  • 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]  
  • 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 [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]  
  • Ouverney, C. C., Fuhrman, J. A. (2000). Marine Planktonic Archaea Take Up Amino Acids. Appl. Environ. Microbiol. 66: 4829-4833 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
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 Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.
Agricola
Right arrow Articles by Cottrell, M. T.
Right arrow Articles by Kirchman, D. L.