Abstract
Most techniques used to assay the growth of microbes in natural communities provide no information on the relationship between microbial productivity and community structure. To identify actively growing bacteria, we adapted a technique from immunocytochemistry to detect and selectively isolate DNA from bacteria incorporating bromodeoxyuridine (BrdU), a thymidine analog. In addition, we developed an immunocytochemical protocol to visualize BrdU-labeled microbial cells. Cultured bacteria and natural populations of aquatic bacterioplankton were pulse-labeled with exogenously supplied BrdU. Incorporation of BrdU into microbial DNA was demonstrated in DNA dot blots probed with anti-BrdU monoclonal antibodies and either peroxidase- or Texas red-conjugated secondary antibodies. BrdU-containing DNA was physically separated from unlabeled DNA by using antibody-coated paramagnetic beads, and the identities of bacteria contributing to both purified, BrdU-containing fractions and unfractionated, starting-material DNAs were determined by length heterogeneity PCR (LH-PCR) analysis. BrdU-containing DNA purified from a mixture of DNAs from labeled and unlabeled cultures showed >90-fold enrichment for the labeled bacterial taxon. The LH-PCR profile for BrdU-containing DNA from a labeled, natural microbial community differed from the profile for the community as a whole, demonstrating that BrdU was incorporated by a taxonomic subset of the community. Immunocytochemical detection of cells with BrdU-labeled DNA was accomplished by in situ probing with anti-BrdU monoclonal antibodies and Texas red-labeled secondary antibodies. Using this suite of techniques, microbial cells incorporating BrdU into their newly synthesized DNA can be quantified and the identities of these actively growing cells can be compared to the composition of the microbial community as a whole. Since not all strains tested could incorporate BrdU, these methods may be most useful when used to gain an understanding of the activities of specific species in the context of their microbial community.
MeSH Terms
Antibodies, Monoclonal/immunology
Bacteria/classification,genetics,growth & development,metabolism
Bromodeoxyuridine/immunology,metabolism
DNA, Bacterial/analysis,biosynthesis,isolation & purification
Ecosystem
Fresh Water
Genes, Bacterial
Genes, rRNA
Immunoblotting
Immunohistochemistry/methods
Immunomagnetic Separation
Phylogeny
Polymerase Chain Reaction/methods
RNA, Ribosomal, 16S/genetics
Water Microbiology
Chemicals
Antibodies, Monoclonal
DNA, Bacterial
RNA, Ribosomal, 16S
Bromodeoxyuridine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Urbach E
Department of Microbiology, Oregon State University, Corvallis, Oregon 97331, USA. urbache@bcc.orst.edu
Vergin K L
Giovannoni S J
References (23)
23 references, click to expand
-
Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific oceans.
Appl Environ Microbiol. 1996 Apr;62(4):1171-7
PMID: 8919778
-
A tentative direct microscopic method for counting living marine bacteria.
Can J Microbiol. 1979 Mar;25(3):415-20
PMID: 378340
-
Utilization of 5-bromouracil by thymineless bacteria.
J Bacteriol. 1967 Jan;93(1):86-9
PMID: 5335905
-
Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (ghosts).
Appl Environ Microbiol. 1995 Jun;61(6):2180-5
PMID: 16535043
-
Thymidine uptake, thymidine incorporation, and thymidine kinase activity in marine bacterium isolates.
Appl Environ Microbiol. 1990 May;56(5):1367-72
PMID: 2160223
-
Genetic diversity in Sargasso Sea bacterioplankton.
Nature. 1990 May 3;345(6270):60-3
PMID: 2330053
-
Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells.
Science. 1989 Mar 10;243(4896):1360-3
PMID: 2466341
-
Bacterial growth rate in the sea: direct analysis by thymidine autoradiography.
Science. 1967 Jan 6;155(3758):81-3
PMID: 6015565
-
Validity of the tritiated thymidine method for estimating bacterial growth rates: measurement of isotope dilution during DNA synthesis.
Appl Environ Microbiol. 1984 Dec;48(6):1076-83
PMID: 6517579
-
Regulation of chromosome replication and segregation in bacteria.
Bacteriol Rev. 1966 Mar;30(1):3-32
PMID: 5324649
-
Comparison of Nucleic Acid Hybridization and Fluorometry for Measurement of the Relationship between RNA/DNA Ratio and Growth Rate in a Marine Bacterium.
Appl Environ Microbiol. 1993 May;59(5):1303-9
PMID: 16348926
-
Use of a fluorescent redox probe for direct visualization of actively respiring bacteria.
Appl Environ Microbiol. 1992 Jun;58(6):1801-8
PMID: 1622256
-
Dual staining of natural bacterioplankton with 4',6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S rRNA sequences.
Appl Environ Microbiol. 1992 Jul;58(7):2158-63
PMID: 1379029
-
Autoradiography and epifluorescence microscopy combined for the determination of number and spectrum of actively metabolizing bacteria in natural water.
Appl Environ Microbiol. 1978 Sep;36(3):506-12
PMID: 83123
-
Determination of Active Marine Bacterioplankton: a Comparison of Universal 16S rRNA Probes, Autoradiography, and Nucleoid Staining.
Appl Environ Microbiol. 1997 Apr;63(4):1208-13
PMID: 16535563
-
A molecular view of microbial diversity and the biosphere.
Science. 1997 May 2;276(5313):734-40
PMID: 9115194
-
Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR.
Appl Environ Microbiol. 1996 Feb;62(2):625-30
PMID: 8593063
-
THE REPLICATION OF DNA IN ESCHERICHIA COLI.
Proc Natl Acad Sci U S A. 1958 Jul 15;44(7):671-82
PMID: 16590258
-
Tolerance to bromodeoxyuridine in a thymidine-requiring strain of Bacillus subtilis.
J Gen Microbiol. 1986 Feb;132(2):481-92
PMID: 2423635
-
Bromodeoxyuridine: a diagnostic tool in biology and medicine, Part I: Historical perspectives, histochemical methods and cell kinetics.
Histochem J. 1995 May;27(5):339-69
PMID: 7657555
-
Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample.
Appl Environ Microbiol. 1997 Mar;63(3):983-9
PMID: 9055415
-
Bacterioplankton secondary production estimates for coastal waters of british columbia, antarctica, and california.
Appl Environ Microbiol. 1980 Jun;39(6):1085-95
PMID: 16345577
-
Identification of bacterial cells by chromosomal painting.
Appl Environ Microbiol. 1997 Mar;63(3):1118-23
PMID: 9055426