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Isolation of Diverse Members of the Aquificales from Geothermal Springs in Tengchong, China

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Isolation of Diverse Members of the Aquificales from Geothermal Springs in Tengchong, China ORIGINAL RESEARCH ARTICLE published: 27 February 2015 doi: 10.3389/fmicb.2015.00157 Isolation of diverse members of the Aquificales from geothermal springs in Tengchong, China Brian P.Hedlund 1,2 *, Anna-Louise Reysenbach 3 *, Liuquin Huang 4 , John C. Ong1, Zizhang Liu 4 , Jeremy A. Dodsworth1,5 , Reham Ahmed 1, Amanda J. Williams1, Brandon R. Briggs 6 , Yitai Liu 3 , Weiguo Hou 4 and Hailiang Dong 4,6 * 1 School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, NV, USA 2 Nevada Institute of Personalized Medicine, University of Nevada, Las Vegas, Las Vegas, NV, USA 3 Biology Department and Center for Life in Extreme Environments, Portland State University, Portland, OR, USA 4 State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing, China 5 Department of Biology, California State University San Bernardino, San Bernardino, CA, USA 6 Department of Geology and Environmental Earth Science, Miami University, Oxford, OH, USA Edited by: The order Aquificales (phylum Aquificae) consists of thermophilic and hyperthermophilic Jesse Dillon, California State bacteria that are prominent in many geothermal systems, including those in Teng- University, USA chong, Yunnan Province, China. However, Aquificales have not previously been isolated Reviewed by: from Tengchong. We isolated five strains of Aquificales from diverse springs (temperature John R. Spear, Colorado School of ◦ Mines, USA 45.2–83.3 C and pH 2.6–9.1) in the Rehai Geothermal Field from sites in which Aquificales Tim McDermott, Montana State were abundant. Phylogenetic analysis showed that four of the strains belong to the genera University, USA Hydrogenobacter, Hydrogenobaculum, and Sulfurihydrogenibium, including strains distant *Correspondence: enough to likely justify new species of Hydrogenobacter and Hydrogenobaculum.The Brian P.Hedlund, School of Life additional strain may represent a new genus in the Hydrogenothermaceae. All strains Sciences, University of Nevada, Las Vegas and Nevada Institute of were capable of aerobic respiration under microaerophilic conditions; however, they had Personalized Medicine, Las Vegas, NV variable capacity for chemolithotrophic oxidation of hydrogen and sulfur compounds and 89154-4004, USA nitrate reduction. e-mail: [email protected]; Anna-Louise Reysenbach, Biology Keywords: Aquificales, Hydrogenobacter, Hydrogenobaculum, Sulfurihydrogenibium, hot springs, hydrogen Department and Center for Life in oxidation, sulfide oxidation, thiosulfate oxidation Extreme Environments, Portland State University, Portland, OR 89154-4004, USA e-mail: [email protected]; Hailiang Dong, State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China e-mail: [email protected] INTRODUCTION are capable of using a variety of inorganic compounds to fuel 2− The phylum Aquificae is composed of a single order, Aquificales, chemolithotrophy, including diverse electron donors (H2,S , 2− 2− 0 2+ 3− and three families, Aquificaceae, Hydrogenothermaceae, and Desul- S2O3 ,SO3 ,S ,Fe ,AsO3 ) and terminal electron accep- − 2− 3+ 3− 2− furobacteriaceae (Reysenbach et al., 2005; L’Haridon et al., 2006). tors (O2,NO3 ,SO3 ,Fe ,AsO4 ,SeO3 ; Stohr et al., 2001; Aquificales are present in many terrestrial and marine geothermal Takai et al., 2001; Eder and Huber, 2002; O’Neill et al., 2008). systems where they often form multicellular “streamer” assem- Two families of Aquificales dominate in terrestrial geother- blages (Huber et al., 1998; Reysenbach et al., 2000, 2005; Takacs mal systems, the Aquificaceae and Hydrogenothermaceae.The et al., 2001; Eder and Huber, 2002; Spear et al., 2005; Hou et al., Aquificaceae includes three genera that are abundant in terrestrial 2013; Takacs-Vesbach et al.,2013) but can also be prominent mem- systems: Hydrogenobacter, Thermocrinis, and Hydrogenobaculum bers of planktonic microbial communities (Cole et al., 2013; Hou (Reysenbach, 2001; Takacs-Vesbach et al., 2013). Hydrogenobac- et al., 2013; Murphy et al., 2013). Most members of the Aquifi- ter and Thermocrinis are closely related and are capable of cales are obligate or facultative autotrophs (Kawasumi et al., 1984; axenic growth at circumneutral pH to ≥85◦C(Kawasumi Stohr et al., 2001; Takai et al., 2001; Eder and Huber, 2002; Aguiar et al., 1984; Takai et al., 2001; Eder and Huber, 2002) and et al., 2004; Caldwell et al., 2010), although at least one isolate was ≥89◦C(Huber et al., 1998; Eder and Huber, 2002; Cald- reported to be incapable of autotrophic growth under the con- well et al., 2010), respectively. In contrast, known isolates ditions that were tested (Takai et al., 2001). Although very few of Hydrogenobaculum are acidophilic (optimum pH 3–4) and studies have quantified autotrophy in terrestrial geothermal sys- have lower growth temperature ranges, with optima between tems inhabited by Aquificales (Boyd et al., 2009), Aquificales are 60 and 70◦C(Shima and Suzuki, 1993; D’Imperio et al., broadly hypothesized to be important primary producers and 2008). The family Hydrogenothermaceae includes a single www.frontiersin.org February 2015 | Volume 6 | Article 157 | 1 Hedlund et al. Diverse Aquificales from Tengchong, China genus that is prominent in many terrestrial geothermal sys- large number of Bacteria and Archaea have been isolated from tems, Sulfurihydrogenibium, with known isolates capable of Rehai springs, particularly thermophilic members of the Firmi- growth to ≥75◦C at circumneutral pH (5.0–8.8; O’Neill et al., cutes (Bacillales, Thermoanaerobales, Clostritiales), Deinococcus- 2008). Thermus phylum (Thermales), and Crenarchaeota (Sulfolobales) Yunnan Province, in southwest China, has a large number of (reviewed in Hedlund et al., 2012). However, despite recent geothermal springs, particularly in Tengchong County, which is cultivation-independent studies suggesting that Aquificales are located within the Indo-Burma Range along the central-western abundant in nearly all high-temperature sites in Rehai (Pagal- border between Yunnan Province and Myanmar. Geothermal ing et al., 2012; Hou et al., 2013; Song et al., 2013; Briggs activity in Yunnan Province is typically located along arched et al., 2014), there are no published reports of the isolation fault structures and circular depressions and is likely fueled by or characterization of Aquificales from Rehai or anywhere in latent heat from tectonic activity associated with the subduc- China. tion of Tethys Ocean lithosphere (Liao and Guo, 1986; Wang In this study, we isolated Aquificales from sites in Teng- et al., 2008). The largest and best-known geothermal area in chong known to host abundant Aquificales populations and sites Tengchong is the Rehai (“Hot Sea”) Geothermal Field, with with abundant streamer growth that were deemed likely to host springs reaching the boiling point (∼95◦Cat∼1,500 m ele- Aquificales. The strains belong to the genera Hydrogenobacter, vation) and spanning a pH range of 2.5–9.4 at high temper- Hydrogenobaculum, and Sulfurihydrogenibium, and possibly a new ature (>80◦C; Figure 1; Table 1; Hedlund et al., 2012). A genus within the Hydrogenothermaceae. Although most of the FIGURE 1 | Study area map and sample locations. Strains were isolated (E) Hydrogenothermaceae strain T-5 from a white/yellow streamer from five hot spring locations in the Rehai Geothermal Field (A) in community in a sulfurous seep on a hillside south of Shuirebaoza, site Yunnan, China: (B) Hydrogenobacter sp. T-2 from a white streamer Srbz-U (70.0◦C, pH 6.6), (F) Sulfurihydrogenibium subterraneum T-7 from a community in Gumingquan (Drum Beating Spring) pool site Gmq-P white/yellow streamer community in Hamazui-3 (spring located ∼5mSE (82.9◦C, pH 8.94), (C) Hydrogenobacter sp. T-8 from Qiao Quan (Bridge of Hamazui), site HMZFJ-3 (68.0◦C, pH 6.50). (A) is modified from Spring) site QQ (74.6◦C, pH 6.36), (D) Hydrogenobaculum sp. T-6 from Hedlund et al. (2012). Fifty mL conical tubes used for scale are 11.7 cm Diretiyanqu (Experimental) site DRTY (60.0◦C, pH 2.62), long. Frontiers in Microbiology | Extreme Microbiology February 2015 | Volume 6 | Article 157 | 2 Hedlund et al. Diverse Aquificales from Tengchong, China Table 1 | Sources of Aquificales strains isolated fromTengchong hot springs and their 16S rRNA gene sequences. Organism* Source location and characteristics Accession numbers Hydrogenobacter sp. T -2 White streamer community in Gumingquan (Drum Beating KP175576 Spring) pool near site Gmq-P (82.9◦C, pH 8.94; GPS N24.95093◦, E98.43626◦) Hydrogenobacter sp. T -8 Small white streamers above iron oxide mat in Qiao Quan KP175579 (Bridge Spring) site QQ (74.6◦C, pH 6.36; GPS N24.95044◦, E98.43650◦) Hydrogenobaculum sp. T -6 Bulk sediment and water Diretiyanqu (Experimental) site KP125885 DRTY (60.0◦C, pH 2.62; GPS N24.95390◦, E98.43819◦) Hydrogenothermaceae strain T -5 White streamer community in sulfurous seep on hillside KP175577 southwest of Shuirebaoza, site Srbz-U (70.0◦C, pH 6.6; GPS N24.95002◦, E98.43743◦) S. subterraneum T -7 Iron oxide mat/streamer community near Hamazui (spring KP175578 located ∼5 m SE of Hamazui) site HMZFJ-1 (68.0◦C, pH 6.50; GPS N24.94992◦, E98.43808◦) *Samples for T-2,T-5,T-7, and T-8 were collected on 07/04/13. The sample for T-6 was collected on 12/29/12. See Figure 1 for photos of sampling sites. strains likely represent new taxa, their general physiological traits consisted of ∼2 L anaerobic chamber gas (N2:CO2:H2 at 90:5:5) are similar to known members of these genera, including variable supplemented with 200 mL H2:CO2 (80:20) and 100 mL air. capacity for aerobic hydrogen oxidation via the“knallgas reaction,” Isolated colonies were re-streaked two times to ensure purity. chemolithotrophic oxidation of sulfur compounds, and anaerobic Strain T-5 was isolated using an extinction-to-dilution method respiration of nitrate. that was repeated at least seven times. For all strains, purity was confirmed through microscopic observation and sequencing of MATERIALS AND METHODS the 16S rRNA gene, following the general approach described SAMPLE COLLECTION, ENRICHMENT, AND ISOLATION previously (Nakagawa et al., 2005).
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