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Molecular Analysis of Deep Subsurface Microbial Communities in Nankai Trough Sediments (ODP Leg 190,Site 1176)

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Molecular Analysis of Deep Subsurface Microbial Communities in Nankai Trough Sediments (ODP Leg 190,Site 1176) FEMS Microbiology Ecology 45 (2003) 115^125 www.fems-microbiology.org Molecular analysis of deep subsurface microbial communities in Nankai Trough sediments (ODP Leg 190,Site 1176) Konstantinos Ar. Kormas a;Ã,David C. Smith b,Virginia Edgcomb a,Andreas Teske a;1 a Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA b Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882, USA Received 19 December 2002; received in revised form 5 April 2003; accepted 14 April 2003 First published online 4 June 2003 Abstract The prokaryotic community inhabiting the deep subsurface sediments in the Forearc Basin of the Nankai Trough southeast of Japan (ODP Site 1176) was analyzed by 16S rDNA sequencing. Sediment samples from 1.15,51.05,98.50 and 193.96 m below sea floor (mbsf) harbored highly diverse bacterial communities. The most frequently retrieved clones included members of the Green non-sulfur bacteria whose closest relatives come from deep subsurface environments,a new epsilon-proteobacterial phylotype,and representatives of a cluster of closely related bacterial sequences from hydrocarbon- and methane-rich sediments around the world. Archaeal clones were limited to members of the genus Thermococcus,and were only obtained from the two deepest samples. ß 2003 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. Keywords: Bacterium; Archaea; 16S rRNA; Marine; Deep subsurface; Ocean Drilling Program; JOIDES resolution; Leg 190; Site 1176; Nankai Trough 1. Introduction of the pure culture isolations and characterizations from deep marine sediments have focused on sulfate-reducing The deep subsurface biospheres of the world’s oceans bacteria from the Japan Sea [6,7] and the Cascadia Margin have only recently become a main focus of scienti¢c re- [8]. Diverse heterotrophic proteobacteria,Gram-positive search. Although approximately 70% of the Earth’s sur- bacteria and members of the Cytophaga^Flavobacte- face is marine,little is known about the microbiology of rium^Bacteroides (CFB) phylum have also been enriched the underlying sediments. Recent estimates of global bac- from deep sediments of the Nankai Trough southeast of terial biomass indicate that a large fraction of bacterial Japan [9]. Likewise,extensive cultivation e¡orts on sam- biomass resides in the deep subsurface,most of which is ples from terrestrial subsurface environments have yielded in the marine deep subsurface [1,2]. predominantly members of the alpha-,beta-,and gamma- Although rates of metabolic processes in the deep-sea proteobacteria,the CFB phylum and of the high G+C and subsurface have been estimated [2^4],the microorganisms low G+C Gram-positive bacteria [10]. To date,almost all remain largely unidenti¢ed. Cultivation surveys and most cultured bacteria from the deep subsurface fall into well- probable number quanti¢cations have detected fermenta- known bacterial genera with many cultured species and tive,nitrate-reducing and sulfate-reducing bacteria as well strains from near-surface habitats. as methanogenic archaea ([5] and references therein). Most A very di¡erent picture emerges from culture-indepen- dent surveys using polymerase chain reaction (PCR),clon- ing and sequencing of rRNA genes and functional genes. From the ¢rst sequencing studies of deep subsurface sedi- * Corresponding author. Present address: Department of Zoology ^ ments [11,12],it has become clear that these microbial Marine Biology,School of Biology,University of Athens,157 84 Pane- ecosystems harbor diverse bacteria and archaea that are pistimiopoli,Athens,Greece. Tel.: +30 (210) 727-4721; Fax: +30 (210) in many cases only distantly related to cultured isolates 727-4604. [13^15]. This 16S rRNA survey describes the prokaryotic E-mail address: [email protected] (K.A. Kormas). biodiversity of non-hydrothermal deep subsurface sedi- 1 Present address: Department of Marine Sciences,Venable Hall 12-1, ments from 1^194 m below sea £oor (mbsf) at a water CB 3300,University of North Carolina,Chapel Hill,NC 27599,USA. depth of 3017 m in the Nankai Trough southeast of Japan. 0168-6496 / 03 / $22.00 ß 2003 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. doi:10.1016/S0168-6496(03)00128-4 FEMSEC 1525 9-7-03 116 K.A. Kormas et al. / FEMS Microbiology Ecology 45 (2003) 115^125 2. Materials and methods mbsf,the sediments are approximately 800 000 years old [19]. The sediments consist predominantly of nannofossil- 2.1. Site description and sampling rich hemipelagic mud interlayered with volcanic ash,and sand-to-silt turbidites showing local soft-sediment folding All sediment samples for this study were obtained dur- and disruption. Diatoms become scarce in the lower part ing Ocean Drilling Program (ODP) Leg 190,from Hole of the unit,but nannofossils are abundant throughout. 1176A in the Nankai Trough,at a depth of 3017 m below This sedimentary sequence is characterized by hemipelagic sea level in June 2000 (Fig. 1). Sediment samples were settling,occasional turbidity currents,and submarine mud retrieved by advanced piston coring (APC),except for £ows,together with air falls of volcanic ash. Porosities the sample from 194 mbsf that was retrieved by extended decrease gradually with depth,from V65^70% at the core barrel (XCB) drilling [16,17]. Using cutting wires, mudline to 55^60% at 220 mbsf,with a steeper decrease whole-round samples were obtained from core sections by 3^5% around 200 mbsf,and remain relatively constant immediately after core retrieval. Subcore samples of ap- between 40 and 45% at 300 mbsf. Temperature increased proximately 706^1178 ml were taken from sediment layers linearly from 1.4‡C at 1.15 mbsf to 12.2‡C at 193.94 mbsf. at 1.15,51.05,98.50 and 193.96 mbsf,and were stored at Sulfate concentrations decreased with depth,and reached 380‡C on the ship until transport to the home laboratory zero at approximately 20 mbsf. Sulfate concentrations de- on dry ice. creased linearly with depth over the upper 10 m,followed Site 1176 is located in the upper slope basin within the by a local maximum at 20 mbsf. At the base of Hole large thrust-slice zone in the Nankai Trough accretionary 1176A (325^393 mbsf),sulfate concentrations increased prism,which is created by the subduction of the sediment- again to V17 mM,almost 60% of the seawater value. rich Philippine plate below the Eurasian plate at a rate of Except for sulfate,pore £uid composition at these depths 4 cm/year [18]. All samples analyzed in the present study remained near that of seawater,suggesting slow,ongoing belong to the same quaternary sediment unit in the upper bacterial sulfate reduction. Ammonium produced by mi- slope basin that covers the accretionary prism. At 200 crobially mediated decomposition of organic matter in- Fig. 1. Location of ODP Site 1176 in relation to other ODP sites on the transect covering the Nankai Trough southeast of Japan. FEMSEC 1525 9-7-03 K.A. Kormas et al. / FEMS Microbiology Ecology 45 (2003) 115^125 117 creased in concentration with depth,having a broad max- primers BAC-8F (5P-AGAGTTTGATCCTGGCTCAG- imum of V5 mM between V20 and 200 mbsf and peaked 3P) and BAC-907R (5P-CCCGTCAATTCCTTTGAGT- at V100 mbsf. Total organic carbon (TOC) ranged from TT-3P) were used. Each PCR run consisted of a 1-min 0.30 to 1.73 wt% in the ¢rst 200 mbsf (lowest at 62.48 and pre-PCR hold at 94‡C,followed by 30 cycles consisting highest at 135.20 mbsf). Headspace gas concentrations of of a 45-s denaturation step at 94‡C,a 45-s annealing step methane were very low in the ¢rst 11.9 mbsf within the at 52.5‡C,a 2-min elongation step at 72‡C,and at the end sulfate reduction zone (7.3^11.7 ppm),increased to 3000^ of the 30 cycles,a ¢nal 7-min ¢nishing step at 72‡C. All 30000 ppm below the sulfate reduction zone,and returned PCR ingredients were prepared with twice-autoclaved ul- to generally less than 10 ppm in the deepest portion of the tra pure water,and stringent anticontamination controls core,below 325 mbsf. Methane was the most dominant were used during PCR preparation. The PCR products hydrocarbon measured throughout Hole 1176A. In gener- were checked on a 1% low-melt agarose gel,bands were al,bacterial cell densities declined rapidly from the sur- excised,and PCR products were extracted with the Prep- face. Microbial abundances,determined by acridine or- A-Gene DNA gel puri¢cation kit (Bio-Rad,Hercules,CA, ange direct counts [2,5],decreased by one order of USA) following the manufacturer’s protocol. The puri¢ed magnitude over the sampling interval from 9.33U107 cells PCR products were A-tailed to improve cloning e⁄ciency per cm3 sediment at 1.19 mbsf to 1.19U107 at 193.94 by mixing approximately 50 ng of puri¢ed PCR product mbsf,followed by a further decrease to 1.11 U106 per with 5 Wlof10UPCR bu¡er (200 mM Tris (pH 8.55),100 3 cm in the two deepest samples at 344 and 363.5 mbsf. mM (NH4)2SO4,20 mM MgCl 2,300 mM KCl,0.1% (wt/ The most intense microbially mediated reactions occurred vol PCR bu¡er) gelatin,0.5% (vol/vol PCR bu¡er) NP- in the top 100 mbsf of the section [19]. 40),5 Wl deoxynucleoside triphosphate (2 mM) and 1 U of Taq DNA polymerase (Promega,Madison,WI,USA). 2.2. DNA isolation, 16S rRNA gene ampli¢cation, cloning The mixture was incubated at 72‡C for 10 min,extracted and sequencing with phenol^chloroform^isoamyl alcohol (25:24:1) and centrifuged for 5 min.
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