Search tips
Search criteria 


Logo of aemPermissionsJournals.ASM.orgJournalAEM ArticleJournal InfoAuthorsReviewers
Appl Environ Microbiol. 1997 January; 63(1): 63–70.
PMCID: PMC168303

Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria.


Small-subunit (SSU) ribosomal DNA (rDNA) gene clusters are phylogenetically related sets of SSU rRNA genes, commonly encountered in genes amplified from natural populations. Genetic variability in gene clusters could result from artifacts (polymerase error or PCR chimera formation), microevolution (variation among rrn copies within strains), or macroevolution (genetic divergence correlated with long-term evolutionary divergence). To better understand gene clusters this study assessed genetic diversity and distribution of a single environmental SSU rDNA gene cluster, the SAR11 cluster. SAR11 cluster genes, from an uncultured group of the alpha subclass of the class Proteobacteria, have been recovered from coastal and midoceanic waters of the North Atlantic and Pacific. We cloned and bidirectionally sequenced 23 new SAR11 cluster 16S rRNA genes, from 80 and 250 m in the Sargasso Sea and from surface coastal waters of the Atlantic and Pacific, and analyzed them with previously published sequences. Two SAR11 genes were obviously PCR chimeras, but the biological (nonchimeric) origins of most subgroups within the cluster were confirmed by independent recovery from separate gene libraries. Using group-specific oligonucleotide probes, we analyzed depth profiles of nucleic acids, targeting both amplified rDNAs and bulk RNAs. Two subgroups within the SAR11 cluster showed different highly depth-specific distributions. We conclude that some of the genetic diversity within the SAR11 gene cluster represents macroevolutionary divergence correlated with niche specialization. Furthermore, we demonstrate the utility for marine microbial ecology of oligonucleotide probes based on gene sequences amplified from natural populations and show that a detailed knowledge of sequence variability may be needed to effectively design these probes.

Full Text

The Full Text of this article is available as a PDF (259K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Amann R, Snaidr J, Wagner M, Ludwig W, Schleifer KH. In situ visualization of high genetic diversity in a natural microbial community. J Bacteriol. 1996 Jun;178(12):3496–3500. [PMC free article] [PubMed]
  • Barns SM, Fundyga RE, Jeffries MW, Pace NR. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1609–1613. [PubMed]
  • Bascuñana CR, Mattsson JG, Bölske G, Johansson KE. Characterization of the 16S rRNA genes from Mycoplasma sp. strain F38 and development of an identification system based on PCR. J Bacteriol. 1994 May;176(9):2577–2586. [PMC free article] [PubMed]
  • Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. [PMC free article] [PubMed]
  • Salama M, Sandine W, Giovannoni S. Development and application of oligonucleotide probes for identification of Lactococcus lactis subsp. cremoris. Appl Environ Microbiol. 1991 May;57(5):1313–1318. [PMC free article] [PubMed]
  • Choi BK, Paster BJ, Dewhirst FE, Göbel UB. Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infect Immun. 1994 May;62(5):1889–1895. [PMC free article] [PubMed]
  • Cilia V, Lafay B, Christen R. Sequence heterogeneities among 16S ribosomal RNA sequences, and their effect on phylogenetic analyses at the species level. Mol Biol Evol. 1996 Mar;13(3):451–461. [PubMed]
  • Dryden SC, Kaplan S. Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res. 1990 Dec 25;18(24):7267–7277. [PMC free article] [PubMed]
  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. [PubMed]
  • Fuhrman JA, McCallum K, Davis AA. Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Appl Environ Microbiol. 1993 May;59(5):1294–1302. [PMC free article] [PubMed]
  • Giovannoni SJ, Britschgi TB, Moyer CL, Field KG. Genetic diversity in Sargasso Sea bacterioplankton. Nature. 1990 May 3;345(6270):60–63. [PubMed]
  • Gordon DA, Giovannoni SJ. Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific oceans. Appl Environ Microbiol. 1996 Apr;62(4):1171–1177. [PMC free article] [PubMed]
  • Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR. Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl Environ Microbiol. 1996 Feb;62(2):668–675. [PMC free article] [PubMed]
  • Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. [PubMed]
  • Kopczynski ED, Bateson MM, Ward DM. Recognition of chimeric small-subunit ribosomal DNAs composed of genes from uncultivated microorganisms. Appl Environ Microbiol. 1994 Feb;60(2):746–748. [PMC free article] [PubMed]
  • Larsen N, Olsen GJ, Maidak BL, McCaughey MJ, Overbeek R, Macke TJ, Marsh TL, Woese CR. The ribosomal database project. Nucleic Acids Res. 1993 Jul 1;21(13):3021–3023. [PMC free article] [PubMed]
  • Maidak BL, Larsen N, McCaughey MJ, Overbeek R, Olsen GJ, Fogel K, Blandy J, Woese CR. The Ribosomal Database Project. Nucleic Acids Res. 1994 Sep;22(17):3485–3487. [PMC free article] [PubMed]
  • Mylvaganam S, Dennis PP. Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics. 1992 Mar;130(3):399–410. [PubMed]
  • Ohkuma M, Kudo T. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol. 1996 Feb;62(2):461–468. [PMC free article] [PubMed]
  • Ohta T. Multigene families and the evolution of complexity. J Mol Evol. 1991 Jul;33(1):34–41. [PubMed]
  • Olsen GJ, Lane DJ, Giovannoni SJ, Pace NR, Stahl DA. Microbial ecology and evolution: a ribosomal RNA approach. Annu Rev Microbiol. 1986;40:337–365. [PubMed]
  • Pedersen K, Arlinger J, Hallbeck L, Pettersson C. Diversity and distribution of subterranean bacteria in groundwater at Oklo in Gabon, Africa, as determined by 16S rRNA gene sequencing. Mol Ecol. 1996 Jun;5(3):427–436. [PubMed]
  • Pettersson B, Johansson KE, Uhlén M. Sequence analysis of 16S rRNA from mycoplasmas by direct solid-phase DNA sequencing. Appl Environ Microbiol. 1994 Jul;60(7):2456–2461. [PMC free article] [PubMed]
  • Pettersson B, Leitner T, Ronaghi M, Bölske G, Uhlen M, Johansson KE. Phylogeny of the Mycoplasma mycoides cluster as determined by sequence analysis of the 16S rRNA genes from the two rRNA operons. J Bacteriol. 1996 Jul;178(14):4131–4142. [PMC free article] [PubMed]
  • Raskin L, Stromley JM, Rittmann BE, Stahl DA. Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol. 1994 Apr;60(4):1232–1240. [PMC free article] [PubMed]
  • Reysenbach AL, Wickham GS, Pace NR. Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl Environ Microbiol. 1994 Jun;60(6):2113–2119. [PMC free article] [PubMed]
  • Robison-Cox JF, Bateson MM, Ward DM. Evaluation of nearest-neighbor methods for detection of chimeric small-subunit rRNA sequences. Appl Environ Microbiol. 1995 Apr;61(4):1240–1245. [PMC free article] [PubMed]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PubMed]
  • Schmidt TM, DeLong EF, Pace NR. Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol. 1991 Jul;173(14):4371–4378. [PMC free article] [PubMed]
  • Shuldiner AR, Nirula A, Roth J. Hybrid DNA artifact from PCR of closely related target sequences. Nucleic Acids Res. 1989 Jun 12;17(11):4409–4409. [PMC free article] [PubMed]
  • Ward DM, Weller R, Bateson MM. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature. 1990 May 3;345(6270):63–65. [PubMed]
  • Woese CR. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. [PMC free article] [PubMed]
  • Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158–2162. [PubMed]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)