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Primary Energy Metabolism in Geothermal Environments:The Role *À>ÀÞÊ iÀ}ÞÊiÌ>LÃÊÊiÌ iÀ>Ê ÛÀiÌÃ\Ê / iÊ,iÊvÊ >ÀLÊÝ`i &RANK42OBB \*UAN-'ONZALEZ\4ATYANA3OKOLOVA\3TEPHEN-4ECHTMANN\.ICOLAI#HERNYH !LEXANDER,EBEDINSKI\,UKE*4ALLON\+RISTIE*ONES\-ARTIN7U\*ONATHAN!%ISEN 4HE#ENTEROF-ARINE"IOTECHNOLOGY "ALTIMORE -$ )NSTITUTODE2ECURSOS.ATURALESY!GROBIOLOGIA #3)# 3EVILLA 3PAIN 7INOGRADSKY)NSTITUTEOF-ICROBIOLOGY 2USSIAN!CADEMYOF3CIENCES -OSCOW 4HE)NSTITUTEFOR'ENOMIC2ESEARCH 2OCKVILLE -$ #ORRESPONDING!UTHOR #ENTEROF-ARINE"IOTECHNOLOGY 5NIVERSITYOF-ARYLAND"IOTECHNOLOGY)NSTITUTE %0RATT3T "ALTIMORE-$ 0HONE&AX%MAILROBB UMBIUMDEDU £È{ "/ ,Ê ""9Ê Ê " -/,9Ê Ê9 "7-/" Ê /" Ê*, -/, / #HEMOLITHOTROPHICMETABOLISMFUELSPRIMARYPRODUCTIONINMANYHYDROTHERMALECOSYSTEMS REPRESENTINGENERGYCONSERVATION STRATEGIESTHATMAYBEINDEPENDENTOFSUNLIGHT-ANYAUTOTROPHICMETABOLICPATHWAYSINGEOTHERMALCOMMUNITIESDEPEND ON(HOWEVER INTHISPAPERWEFOCUSONANAEROBICCARBOXYDOTROPHSTHATARECAPABLEOFUSING#/ASACARBONANDENERGY SOURCE PRODUCING ( AND #/ 7E HAVE RECENTLY COMPLETED THE GENOME SEQUENCE OF AN AUTOTROPHIC CARBOXYDOTROPH #ARBOXYDOTHERMUSHYDROGENOFORMANS WHICHAPPEARSTOBEASPECIALISTIN#/ OXIDATION ENCODINGlVEUNLINKEDGENETICLOCI CAPABLEOFEXPRESSING#/DEHYDROGENASE"ECAUSEOFTHEIRGLOBALOCCURRENCEINGEOTHERMALENVIRONMENTS WEPROPOSETHAT #/ UTILIZINGORGANISMSPLAYIMPORTANTROLESINANAEROBICMICROBIALCONSORTIA4OUNDERSTANDTHEROLEOF#/ UTILIZINGBACTERIA IN9ELLOWSTONEHOTSPRINGSWEISOLATEDANDDESCRIBEDANOVEL( PRODUCINGBACTERIUMSTRAIN.OR FROMAN&E RICHSITEIN .ORRIS'EYSER"ASIN 9.03TRAIN.ORISALOW ' #'RAM POSITIVEBACTERIUMBELONGINGTOTHEDIVISION&IRMICUTES AND O GROWSCHEMOLITHOTROPHICALLYAT #ON#/GENERATIONTIMEH PRODUCINGEQUIMOLARQUANTITIESOF(AND#/3TRAIN .ORISALSOCAPABLEOFCHEMOAUTOTROPHICGROWTHON&E)))AND3E ASWELLASGROWINGHETEROTROPHICALLYONGLUCOSEANDSEVERAL SUGARS PRODUCINGACETATE ( AND#/7EHAVEPROPOSEDTHATSTRAIN.ORBEASSIGNEDTOANEWGENUS 4HERMOSINUSGENNOV 4HETYPESPECIESIS4HERMOSINUSCARBOXYDIVORANSSPNOVTYPESTRAIN .OR4$3-43OKOLOVAETAL )TISEVIDENT THAT#/ DEPENDENTHYDROGENOGENICMETABOLISMOCCURSINADIVERSEPHYLOGENETICCONTEXTANDCANBEACCOMPANIEDBYAVARIED REPERTOIREOFALTERNATIVETROPHICSTRATEGIES iÞÊ7À`à >>iÀLV V>ÀLÊÝ`i V>ÀLÊÝ`iÊ`i Þ`À}i>Ãi Þ`À}i ÀÊÀi`ÕVÌ ÀÀÃÊiÞÃiÀÊ >à Primary Energy Metabolism in Geothermal Environments 165 1.0 INTRODUCTION darkness will ensue each day at sunset in the natural Over the past two decades, there has been an enormous environment! The CO dehydrogenase and associated increase in the number of new thermophilic isolates with hydrogenase components are repressed by light and diverse metabolic strategies, consistent with the diversity induced by CO and darkness, and growth proceeds at of geochemical energy sources associated with continental a slow rate in the absence of light with a relatively low and submerged hydrothermal vents (reviewed in growth yield coefficient of 3.7 g (dry wt.) of cells per mol Reysenbach and Shock 2002). These metabolic pathways of CO oxidized (Champine and Uffen 1987). fuel chemolithoautotrophic primary production in many Thermophilic CO-utilizers produce H , acetate, or hydrothermal ecosystems such as hot springs in Yellowstone 2 methane as their primary end products, and it seems National Park (YNP) where opportunistic microbial reasonable to assume that they are involved in cross- metabolic adaptation is on display, often in brilliant color. feeding other chemolithotrophs such as methanogens, Carboxydotrophic bacterial thermophiles capable of using acetoclastic methanogens, methanotrophs, H2-oxidizers, or CO(g) as their only source of energy and carbon have S-reducers. This chapter reviews the distribution of several been isolated from diverse geothermal habitats worldwide CO-utilizing thermophiles and describes the isolation of a (Sokolova et al. 2004; Table 1). This unique physiology CO-utilizing organism from Norris Geyser Basin, YNP. is not new to microbiology. First described by Uffen (1976), many phototrophic purple nonsulfur bacteria, 2.0 MATERIALS AND METHODS when cultured anaerobically in the dark, produce H at the 2 2.1 Strains expense of CO, which is converted to CO2. Using tritiated Carboxydothermus hydrogenoformans DSM 6008 water, Uffen showed that H2 was the product in what is and Thermoterrabacterium ferrireducens DSM 11255 now known as the water-gas shift reaction [CO + H2O = were obtained from the Deutsche Sammlung von CO2 + H2]. In these phototrophs, the oxidation of CO appears to be a backup metabolic strategy allowing the Mikroorganismen und Zellkulturen (Braunschweig, cells to maintain a slow growth rate on CO. In effect, the Germany). T. ferrireducens was cultured under strictly capacity for using an alternative energy source represents anaerobic conditions on modified freshwater medium, an important adaptation that, in the case of phototrophs, containing 30 mM glycerol as an electron donor and appears to be justified by the reliable assumption that carbon source, and 20 mM Na-fumarate as an electron Table 1. CO-oxidizing hydrogenogenic microorganisms and their isolation locales. GenBank Organism Isolation Locale Habitat Reference Accession No. Kunashir, Kuril Islands Mud from hot Svetlichnyi et al. Carboxydothermus hydrogenoformans NC_002972 Kamchatka swamp, 68°C, pH 5.5 1991 Raoul Island, Kermadeck Littoral hydrothermal Svetlichnyi et al. Carboxydothermus restrictus Not Available Archipelago sample 1994 Gezyer Valley, Terrestrial hot spring, Carboxydocella thermautotrophica AY061974 Sokolova et al. 2002 Kamchatka 60°C, pH 8.6 Terrestrial hot spring, Thermosinus carboxydivorans AY519200 Norris Basin, YNP, USA Sokolova et al. 2004 50°C, pH 7.5 Thermococcus sp. AM4 AJ583507 East Pacific Rise (13o N) Hydrothermal vent Sokolova et al. 2004 Caldanaerobacter subterraneus subsp. Marine hydrothermal Sokolova et al. 2001; AF120479 Okinawa Trough pacificus vent, 110-130°C Fardeau et al. 2004 Caldanaerobacter subterraneus Not Available Kunashir, Kuril Islands Terrestrial hot spring Subbotina et al. 2003 strain 2707 166 GEOTHERMAL BIOLOGY AND GEOCHEMISTRY IN YELLOWSTONE NATIONAL PARK acceptor. C. hydrogenoformans strain Z-2901 (DSM 6008) the cooS gene from C. hydrogenoformans. Phylogenetic was grown as previously described (Svetlichny et al. 1991). analyses were performed by the program Pileup (Genetic T. ferrireducens was mass cultured in a 200 L fermentor Computer Group) and CLUSTAL W. Bootstrap values at the Center of Marine Biotechnology ExSUF facility, were the percentages from a sampling of 1000. The genome o under a gas phase of 100% CO2 at 65 C. Late exponential sequencing project was conducted in collaboration with phase cells were harvested by centrifugation. The cell J. Eisen and colleagues at The Institute for Genomic paste, containing 150 g of cells (wet wt.), was frozen at Research (TIGR), and the primers devised by A. Lebedinski -80oC for purification of the Fe reductase. at the Russian Academy of Sciences in Moscow. 2.2 Sequencing Studies 2.3 Sampling An earlier study presented results of a genome survey Samples were collected from Norris Geyser Basin, within of C. hydrogenoformans strain Z-2901 (Gonzalez and the One Hundred Spring Plain, during June 2000 (Figure Robb 2000). Genomic DNA was extracted from cultures 1). A sample of sediment and geothermal water was of C. hydrogenoformans strain Z-2901 (DSM 60008), collected from a small geothermal pool containing visible and a genomic library was prepared using lambda Zip- organic matter, at ~ neutral pH (7.5) and a temperature Lox, EcoRI arms (Gibco BRL). Gene walking using the of 50oC (lat 44o43ʹ797ʺN, long 110o42ʹ506ʺW). The Vectorette II system (Genosys) and the CooS specific samples were used as inoculum for the isolation of CO- primer 5ʹ-CCA TCG ATA CTT TCA AAC GGC utilizing organisms using cultivation strategies defined GC-3ʹ was performed to complete the sequence of previously (Sokolova et al. 2004). A B 3.0 RESULTS AND DISCUSSION 3.1 Insights from Sequencing Studies The complete genome sequence of C. hydrogenoformans has provided a gene inventory of a specialized thermophilic carboxydotroph. C. hydrogenoformans was originally described as growing only on CO and pyruvate (Svetlichny et al. 1991). A recent study (Henstra and Stams 2004) C D indicates that C. hydrogenoformans displays more versatile substrate utilization than previously suspected. For example, 9,10- anthraquinone-2,6-disulfonate (AQDS) can act as an alternative to protons as an electron acceptor, where the strain utilizes CO and grows at the normal rate but produces no H2. One of the most unusual features of the annotated C. hydrogenoformans Z-2901 Figure 1. Sampling locations in Yellowstone National Park used for genome sequence is the presence of five enrichment of anaerobic CO-oxidizing strains. A, B. One Hundred Spring Plain, Norris Geyser Basin, showing the hot spring (80-95oC) containing FeIII oxides from dissimilar and apparently paralogous cooS which Thermosinus carboxydovorans was isolated. Sampling equipment shown genes (Figure 2). The operon encoding in B includes temperature probe, pH meter, and altimeter/barometer. C. Sampling CODH I is homologous and similar in location at Potts Basin. D. High temperature sampling with telescopic probe at full extension. gene order and content to the locus in Primary Energy Metabolism in Geothermal Environments 167 Rhodospirillum rubrum, which is induced # 1 2 3 4 5 by growth in the dark in the presence of 0 0.5 1.0 1.5 2.0 2.5 Mb CO. The occurrence of a cooA gene that cooS encodes a heme-containing transcriptional activator protein with marked similarity to a family of cAMP sensor proteins is of significant interest (Roberts et al.
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