Activity of abundant and rare bacteria in a coastal ocean
Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved June 20, 2011 (received for review January 25, 2011)
Abstract
The surface layer of the oceans and other aquatic environments contains many bacteria that range in activity, from dormant cells to those with high rates of metabolism. However, little experimental evidence exists about the activity of specific bacterial taxa, especially rare ones. Here we explore the relationship between abundance and activity by documenting changes in abundance over time and by examining the ratio of 16S rRNA to rRNA genes (rDNA) of individual bacterial taxa. The V1–V2 region of 16S rRNA and rDNA was analyzed by tag pyrosequencing in a 3-y study of surface waters off the Delaware coast. Over half of the bacterial taxa actively cycled between abundant and rare, whereas about 12% always remained rare and potentially inactive. There was a significant correlation between the relative abundance of 16S rRNA and the relative abundance of 16S rDNA for most individual taxa. However, 16S rRNA:rDNA ratios were significantly higher in about 20% of the taxa when they were rare than when abundant. Relationships between 16S rRNA and rDNA frequencies were confirmed for five taxa by quantitative PCR. Our findings suggest that though abundance follows activity in the majority of the taxa, a significant portion of the rare community is active, with growth rates that decrease as abundance increases.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the Short Read Archive in the GenBank database (accession no. SRA037201 and sample accessions nos. SRS211106–SRS211108, SRS211110, and SRS211116–SRS211146).
Acknowledgments
We thank M. Cottrell for assistance with sampling and analyses, W. Nelson for bioinformatic assistance, and M. Oliver for helpful discussions. This work was supported by National Science Foundation Grants MCB-0453993 (to D.L.K.), OCE-0825468 (to B.J.C. and D.L.K), OCE-0824981 (to J.F.H.), and a Partner University Fund grant (to D.L.K.).
Supporting Information
Supporting Information (PDF)
Supporting Information
- Download
- 405.00 KB
References
1
ML Sogin, et al., Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103, 12115–12120 (2006).
2
C Pedrós-Alió, Marine microbial diversity: Can it be determined? Trends Microbiol 14, 257–263 (2006).
3
RR Malmstrom, MT Cottrell, H Elifantz, DL Kirchman, Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Appl Environ Microbiol 71, 2979–2986 (2005).
4
SE Jones, JT Lennon, Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci USA 107, 5881–5886 (2010).
5
BB Ward, Nitrification and the marine nitrogen cycle. Microbial Ecology of the Oceans, ed DL Kirchman (Wiley-Liss, New York), pp. 427–453 (2000).
6
JP Zehr, HW Paerl, Molecular ecological aspects of nitrogen fixation in the marine environment. Microbial Ecology of the Oceans, ed DL Kirchman (Wiley, 2nd Ed, Hoboken, NJ), pp. 481–526 (2008).
7
K Hamasaki, A Taniguchi, Y Tada, RA Long, F Azam, 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 (2007).
8
MS Rappé, SA Connon, KL Vergin, SJ Giovannoni, Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002).
9
SJ Giovannoni, et al., Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005).
10
BJ Campbell, L Yu, TRA Straza, DL Kirchman, Temporal changes in bacterial rRNA and rRNA genes in Delaware (USA) coastal waters. Aquat Microb Ecol 57, 123–135 (2009).
11
R Lami, JF Ghiglione, Y Desdevises, NJ West, P Lebaron, Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA-16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat Microb Ecol 54, 199–210 (2009).
12
F Fegatella, J Lim, S Kjelleberg, R Cavicchioli, Implications of rRNA operon copy number and ribosome content in the marine oligotrophic ultramicrobacterium Sphingomonas sp. strain RB2256. Appl Environ Microbiol 64, 4433–4438 (1998).
13
L Kerkhof, P Kemp, Small ribosomal RNA content in marine Proteobacteria during non-steady-state growth. FEMS Microbiol Ecol 30, 253–260 (1999).
14
MP Deutscher, Degradation of RNA in bacteria: Comparison of mRNA and stable RNA. Nucleic Acids Res 34, 659–666 (2006).
15
PF Kemp, S Lee, J Laroche, Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol 59, 2594–2601 (1993).
16
H Schäfer, et al., Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: Changes in the genetic diversity of bacterial populations. FEMS Microbiol Ecol 34, 243–253 (2001).
17
G Gentile, et al., Study of bacterial communities in Antarctic coastal waters by a combination of 16S rRNA and 16S rDNA sequencing. Environ Microbiol 8, 2150–2161 (2006).
18
E Gaidos, A Rusch, M Ilardo, Ribosomal tag pyrosequencing of DNA and RNA from benthic coral reef microbiota: Community spatial structure, rare members and nitrogen-cycling guilds. Environ Microbiol 13, 1138–1152 (2011).
19
JA Gilbert, et al., The seasonal structure of microbial communities in the Western English Channel. Environ Microbiol 11, 3132–3139 (2009).
20
JA Fuhrman, et al., Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103, 13104–13109 (2006).
21
AH Treusch, et al., Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3, 1148–1163 (2009).
22
C Winter, T Bouvier, MG Weinbauer, TF Thingstad, Trade-offs between competition and defense specialists among unicellular planktonic organisms: The “killing the winner” hypothesis revisited. Microbiol Mol Biol Rev 74, 42–57 (2010).
23
DL Kirchman, MT Cottrell, C Lovejoy, The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ Microbiol 12, 1132–1143 (2010).
24
B van den Bogert, WM de Vos, EG Zoetendal, M Kleerebezem, Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl Environ Microbiol 77, 2071–2080 (2011).
25
PA del Giorgio, JM Gasol, Physiological structure and single-cell activity in marine bacterioplankton. Microbial Ecology of the Oceans, ed DL Kirchman (Wiley-Blackwell, Hoboken, NJ), pp. 243–298 (2008).
26
FM Lauro, et al., The genomic basis of trophic strategy in marine bacteria. Proc Natl Acad Sci USA 106, 15527–15533 (2009).
27
S Yooseph, et al., Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468, 60–66 (2010).
28
E Teira, S Martinez-Garcia, C Lonborg, XA Alvarez-Salgado, Growth rates of different phylogenetic bacterioplankton groups in a coastal upwelling system. Environ Microbiol Rep 1, 545–554 (2009).
29
ML Coleman, SW Chisholm, Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107, 18634–18639 (2010).
30
MS Schwalbach, HJ Tripp, L Steindler, DP Smith, SJ Giovannoni, The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12, 490–500 (2010).
31
J McCarren, et al., Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA 107, 16420–16427 (2010).
32
R Mikkola, CG Kurland, Is there a unique ribosome phenotype for naturally occurring Escherichia coli? Biochimie 73, 1061–1066 (1991).
33
BJ Campbell, SW Polson, TE Hanson, MC Mack, EAG Schuur, The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12, 1842–1854 (2010).
34
M Middelboe, K Holmfeldt, L Riemann, O Nybroe, J Haaber, Bacteriophages drive strain diversification in a marine Flavobacterium: Implications for phage resistance and physiological properties. Environ Microbiol 11, 1971–1982 (2009).
35
M Hamady, JJ Walker, JK Harris, NJ Gold, R Knight, Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5, 235–237 (2008).
36
PD Schloss, et al., Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75, 7537–7541 (2009).
37
Q Wang, GM Garrity, JM Tiedje, JR Cole, Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73, 5261–5267 (2007).
38
S Audic, JM Claverie, The significance of digital gene expression profiles. Genome Res 7, 986–995 (1997).
39
KE Ashelford, AJ Weightman, JC Fry, PRIMROSE: A computer program for generating and estimating the phylogenetic range of 16S rRNA oligonucleotide probes and primers in conjunction with the RDP-II database. Nucleic Acids Res 30, 3481–3489 (2002).
Information & Authors
Information
Published in
Cover image: Pictured is a wing imaginal disc, a larval structure that gives rise to the wing of the adult fruit fly, Drosophila melanogaster. Here, cells expressing a GFP-tagged Hedgehog protein, known to regulate development in a variety of tissue types, are shown in green; cells harboring a mutation in dispatched (disp), a gene required for the export of Hedgehog, are marked by an absence of blue staining. Colocalization staining (red) indicates that Hedgehog accumulates at the outer surface of disp mutant cells. Ainhoa Callejo et al. report that, while Hedgehog is released at both the apical and basolateral membranes of the disc epithelium, only protein released at the basolateral side forms the Hedgehog gradient. See the Feature Article by Callejo et al. on pages 12591–12598. Image courtesy of Isabel Guerrero.
Classifications
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the Short Read Archive in the GenBank database (accession no. SRA037201 and sample accessions nos. SRS211106–SRS211108, SRS211110, and SRS211116–SRS211146).
Submission history
Published online: July 18, 2011
Published in issue: August 2, 2011
Keywords
Acknowledgments
We thank M. Cottrell for assistance with sampling and analyses, W. Nelson for bioinformatic assistance, and M. Oliver for helpful discussions. This work was supported by National Science Foundation Grants MCB-0453993 (to D.L.K.), OCE-0825468 (to B.J.C. and D.L.K), OCE-0824981 (to J.F.H.), and a Partner University Fund grant (to D.L.K.).
Notes
This article is a PNAS Direct Submission.
Authors
Competing Interests
The authors declare no conflict of interest.
Metrics & Citations
Metrics
Citation statements
Altmetrics
Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.
Cited by
Loading...
View Options
View options
PDF format
Download this article as a PDF file
DOWNLOAD PDFLogin options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.