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Remarkable Archaeal Diversity Detected in a Yellowstone National Park Hot Spring Environment (Archaebacteria/Phylogeny/Thermophfly/Molecular Ecology) SUSAN M

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Remarkable Archaeal Diversity Detected in a Yellowstone National Park Hot Spring Environment (Archaebacteria/Phylogeny/Thermophfly/Molecular Ecology) SUSAN M Proc. Nati. Acad. Sci. USA Vol. 91, pp. 1609-1613, March 1994 Microbiology Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment (archaebacteria/phylogeny/thermophfly/molecular ecology) SUSAN M. BARNS, RUTH E. FUNDYGA, MATTHEW W. JEFFRIES, AND NORMAN R. PACE* Department of Biology and Institute for Molecular and Cellular Biology, Indiana University, Bloomington, IN 47405 Contributed by Norman R. Pace, November 17, 1993 ABSTRACT Ofthe three primary phylogenetic domains to amplify archaeal and eucaryal genes selectively. Amplifi- Archaea (archaebacteria), Bacteria (eubacteria), and Eucarya cation products were then cloned and the nucleotide se- (eukaryotes) -Archaea is the least understood in terms of its quences of the inserts were determined.t rDNA sequences diversity, physiologies, and ecological panorama. Although obtained were aligned with and compared to an extensive many species of Crenarchaeota {one of the two recognized data base of rRNA sequences from cultivated species. This archaeal kingdoms sensu Woese [Woese, C. R., Kandler, 0. & report describes the recovery, from this single hot spring, of Wheelis, M. L. (1990) Proc. Nadl. Acad. Sci. USA 87, 4576- rDNA clones from a remarkable variety of archaeal types, 4579J} have been isolated, they constitute a relatively tight-knit many of them crenarchaeal species with no known close cluster oflineages in phylogenetic analyses of rRNA sequences. relatives. It seemed possible that this limited diversity is merely apparent and reflects only a failure to culture organisms, not their absence. We report here phylogenetic characterization ofmany MATERIALS AND METHODS archaeal small subunit rRNA gene sequences obtained by Biomass Collection and DNA Extraction. Samples of the polymerase chain reaction amplification of mixed population upper 1-10 mm ofsediment were collected, frozen on dry ice, DNA extracted directly from sediment of a hot spring in and stored at -70'C until processed. Nucleic acids were Yellowstone National Park. This approach obviates the need extracted from sediment samples by a direct lysis procedure for cultivation to identify organisms. The analyses document adapted from several methods (2-6) and designed to obtain the existence not only ofspecies belonging to well-characterized DNA from a broad range of cell types. Approximately 5 ml crenarchaeal genera or families but also ofcrenarchaeal species of sediment was resuspended in buffer A (500 mM Tris-HCl, for which no close relatives have so far been found. The large pH 8.0/100 mM NaCl/1 mM sodium citrate) in the presence number of distinct archaeal sequence types retrieved from this of polyadenosine (100 pg/ml) and lysozyme (5 mg/ml) and single hot spring was unexpected and demonstrates that Cre- incubated for 1 hr at 370C with occasional agitation. Protein- narchaeota is a much more diverse group than was previously ase K was then added to 2 mg/ml, and the mixture was suspected. The results have impact on our concepts of the incubated for a further 30 min. At the end of incubation, 8 ml phylogenetic organization of Archaea. of lysis buffer [200 mM Tris HCl, pH 8.0/100 mM NaCl/4% (wt/vol) SDS/10% (wt/vol) 4-aminosalicylate] was added, Microbiologists have long understood the limitations of cul- and the solution was mixed gently by inversion. Three cycles tivation techniques in assessing the diversity of naturally of freezing in a dry ice-ethanol bath and thawing in a 650C occurring microbial communities. Commonly, only a small water bath were conducted to release nucleic acids. The fraction of organisms observed microscopically can be cul- mixture was then extracted with an equal volume of phenol tivated using standard methods. Recently, sequence-based [saturated with 100 mM Tris-HCl (pH 8.0)], followed by phylogenetic techniques have been used to alleviate the extraction with phenol/chloroform/isoamyl alcohol, 24:24:1 requirement for cultivation to identify microorganisms. Such (vol/vol). Four grams of acid-washed polyvinylpolypyrroli- studies have detected the presence of previously unknown done (PVPP) (Sigma) (6) was added to the aqueous phase, and organisms in each instance of their use (for review, see ref. the mixture was incubated 30 min at 37TC. The PVPP was 1). These techniques sample microbial populations directly pelleted from the mixture by centrifugation, and the resultant through isolating and sequencing specific genes from the supernatant was filtered through a 0.45-gm (pore size) filter environment. Phylogenetic comparative analysis of these to remove residual PVPP. Bulk nucleic acids were precipi- sequences is then used to determine evolutionary relation- tated from solution with isopropyl alcohol and centrifugation. ships between members of the community and cultivated The resulting pellet was resuspended in 500 jLd of TE (10 mM species. The results allow inference of some properties of Tris HCl, pH 8.0/1 mM EDTA), 0.1 g of anhydrous ammo- otherwise unknown organisms in the environment, based on nium acetate was added, and the solution was mixed quickly the properties of their studied relatives. In addition, the and then centrifuged immediately for 30 min at 40C in a sequences can be used to design oligonucleotide probes for microcentrifuge. Nucleic acids were precipitated from the determination of morphotype and abundance of particular supernatant by addition of 1 vol of isopropyl alcohol, incu- organisms and for assistance in cultivation efforts. bated on ice for 10 min, and centrifuged for 30 min. After We have employed molecular phylogenetic techniques to resuspension in TE, high molecular weight DNA was isolated investigate the diversity of Archaea in a hot spring in Yel- from the extract by purification on Sephadex G-200 (Phar- lowstone National Park. Small-subunit rRNA genes were amplified by polymerase chain reaction (PCR) from DNA Abbreviation: RDP, Ribosomal Database Project. extracted directly from sediment, by using primers designed *To whom reprint requests should be addressed. tThe sequences reported in this paper have been deposited in GenBank data base (accession nos. pJP 6, L25306; pJP 7, L25307; The publication costs ofthis article were defrayed in part by page charge pJP 8, L25309; pJP 9, L25308; pJP 27, L25852; pJP 33, L25300; pJP payment. This article must therefore be hereby marked "advertisement" 41, L25301; pJP 74, L25302; pJP 78, L25303; pJP 81, L25304; pJP in accordance with 18 U.S.C. §1734 solely to indicate this fact. 89, L25305). 1609 Downloaded by guest on October 4, 2021 1610 Microbiology: Barns et al. Proc. Natd. Acad. Sci. USA 91 (1994) macia) columns as described (2) or by size selection on 1% order was randomized in neighbor joining, parsimony, and low-melting-point agarose gels (SeaPlaque GTG, FMC), ac- maximum likelihood analyses. cording to the manufacturer's protocols. Location and Chemical Analysis ofHot Spring. The location PCR Amplition of rDNA. Bulk DNA from Sephadex of the hot spring analyzed in this study was determined using fractions or in agarose gel slices was titrated in amplification a PYXIS IPS-360 global positioning system receiver (Sony). reaction mixtures to empirically determine the optimal DNA Ten readings at 30-s intervals were taken on 2 days and concentration for maximum synthesis of 1- to 1.5-kb prod- averaged to give position ofsite. Water and sediment samples ucts. rRNA genes were amplified by PCR under conditions as were analyzed for chemical composition and pH by WW described (7), with inclusion ofacetamide to 5% (wt/vol) and Analytical Sciences (Cleveland, TN) and by H. Huber (Uni- the substitution of a Tricine-containing buffer (300 mM versity of Regensberg, Germany). Tricine, pH 8.4/500 mM KCI/15 mM MgCl2) (8) for the lOx reaction buffer. After an initial 5-min denaturation at 94TC, during which the DNA polymerase was added, thermal RESULTS cycling conditions were as follows: denaturation at 940C for The hot spring analyzed in this study, "Jim's Black Pool," is 1.5 min, annealing at 55TC for 1.5 min, and extension at 720C located in the Mud Volcano area of Yellowstone National for 2 min, repeated for a total of 40 cycles. The oligonucle- Park, Wyoming, "-0.75 miles (1 mile = 1584 m) southsouth- otide primer sequences used were 1391R (9) (5'-GACG- west of Black Dragon's Cauldron, at 440 36' 35.4" ± 1.3" N GGCGGTGTGTRCA-3') and 23FPL (5'-GCGGATCCGCG- and 110° 26' 20.6" ± 1.3" W. The pool of the spring is GCCGCTGCAGAYCTGGTYGATYCTGCC-3'), where R is approximately 3 x 9 m in size, with several boiling source a purine and Y is a pyrimidine. areas (930C). The water and sediment of the spring are deep Purifiction and Clning of PCR Products. Amplified DNA black in color due to a fine black particulate material, from 5 to 10 reaction mixtures was pooled, heated to 650C to obsidian sand, and possibly iron sulfide, which also accumu- melt agarose if necessary, then extracted sequentially with lates on the periphery ofthe pool. Chemical analysis ofwater phenol/chloroform/isoamyl alcohol and chloroform/isoamyl and sediment samples taken from this pool indicates that it is alcohol, and precipitated with ethanol. After centrifugation, similar in chemistry to other Yellowstone hot springs (see ref. DNA pellets were resuspended in TE and products of the 17), although the sediment contains an unusually high iron expected size (1.4 kb) were purified on 4% polyacrylamide content (415,600 mg/kg). Sulfide is present. Temperature gels, eluted into 300 mM sodium acetate/0.1% SDS, and varies across the pool and increases rapidly with increasing precipitated with ethanol. Products were then digested with depth through the sediment. The sediment was =740C at the restriction endonuclease Not I (New England Biolabs) (10), site of sampling, while pH was approximately neutral (water purified on low-melting-point agarose gels (1% SeaPlaque, pH = 6.7 at 18TC and sediment pH = 7.6 at 20TC).
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