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Halophilic Archaea Determined from Geothermal Steam Vent Aerosols

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Halophilic Archaea Determined from Geothermal Steam Vent Aerosols Environmental Microbiology (2008) 10(6), 1582–1590 doi:10.1111/j.1462-2920.2008.01574.x Halophilic Archaea determined from geothermal steam vent aerosols Dean G. Ellis, Richard W. Bizzoco and Introduction Scott T. Kelley* Fumaroles discharge steam at temperatures up to 180°C Department of Biology, San Diego State University, (Ferreira and Oskarsson, 1999), and the vapour formed San Diego, CA 92182, USA. proceeds directly into the air from the subsurface, often passing through a chimney where vapour and soil contact Summary may occur (Brombach et al., 2000). The upper limit for microbial growth has been reported at 121°C (Kashefi and Hydrothermal vents, known as ‘fumaroles’, are ubiq- Lovley, 2003), and both archaeal and bacterial 16S rRNA uitous features of geothermal areas. Although their gene sequences have been found at temperatures geology has been extensively characterized, little is exceeding 300°C in deep sea hydrothermal vents (Atkin- known about the subsurface microbial ecology of son et al., 2000; Takai et al., 2001; Robinson et al., 2005). fumaroles largely because of the difficulty in collect- Thus, in spite of the extreme heat of fumarole steam, the ing sufficient numbers of cells from boiling steam subsurface zone of vapour formation may harbour micro- water for DNA extraction and culture isolation. Here organisms able to disperse along with the steam water. we describe the first collection, molecular analysis Fumaroles are a ubiquitous feature of geothermal envi- and isolation of microbes from fumarole steam ronments, and although the geology of fumaroles has waters in Russia (Kamchatka) and the USA (Hawaii, been studied extensively, little is known about the micro- New Mexico, California and Wyoming). Surprisingly, biota of fumaroles. Numerous studies have explored the steam vent waters from all the fumaroles the microbial diversity of geothermal springs and pools contained halophilic Archaea closely related to the (Burton and Norris, 2000; Benlloch et al., 2001; Blank Haloarcula spp. found in non-geothermal salt mats, et al., 2002; Norris et al., 2002; Spear et al., 2005) but, to saline soils, brine pools and salt lakes around the our knowledge, only one study has detected microbes world. Microscopic cell counting estimated the cell in geothermal steam water and not from a fumarole dispersal rate at approximately 1.6 ¥ 109 cells year-1 (Bonheyo et al., 2005). The principle difficulty in studying from a single fumarole. We also managed to enrich the microbial constituents in geothermal steam has been microbes in high-salt media from every vent sample, the challenge of collecting sufficient quantities of steam and to isolate Haloarcula from a Yellowstone vent in water for analyses. For example, the recent effort by a 20% salt medium after a month-long incubation, Bonheyo and colleagues (2005) to identify microbes in demonstrating both salt tolerance and viability steam from flowing springs managed to collect only 20 of cells collected from high-temperature steam. cells in ~72 h. Laboratory tests determined that microbes enriched In this article, we describe the successful deployment of in salt media survived temperatures greater than a highly efficient and portable steam collector designed 75°C for between 5 and 30 min during the collection for sterile microbiological sampling of fumarole steam process. Hawaiian fumaroles proved to contain the water (Fig. 1). Fumarole steam is extremely hot and very greatest diversity of halophilic Archaea with four diffuse (see example site photo, Fig. 1C), making it chal- new lineages that may belong to uncultured haloar- lenging to collect in large enough quantities for microbio- chaeal genera. This high diversity may have resulted logical analysis. Our device, which uses temperature from the leaching of salts and minerals through the differentials to condense steam into gamma-irradiated highly porous volcanic rock, creating a chemically polypropylene centrifuge tubes (Fig. 1B), collected up to complex saline subsurface. 4mlmin-1 of fumarole steam water from vents with steam as hot as 93.5°C. After collecting steam water, we used both culture-based and culture-independent methods to determine the identity and viability of cells in steam from Received 20 February, 2007; accepted 26 January, 2008. *For correspondence. E-mail [email protected]; Tel. (+1) 619 thermal habitats in Russia (Kamchatka) and in the USA 594 5371; Fax (+1) 619 594 5676. (Hawaii, New Mexico, California and Wyoming). In this © 2008 The Authors Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd Archaea in fumaroles 1583 Fig. 1. Fumarole collection images. A. Portable steam collector, side view; height = 15 cm, diameter = 10 cm. B. Top view with cover off showing placement of orange-capped sterile 50 ml conical polypropylene tubes. C. Photo of Roaring Mountain site showing example fumarole steam vents alongside the spring water channel. study, we focused on identification and isolation of Results and discussion Archaea, a group including organisms that survive the Sample collection highest known temperature extremes (Blöchl et al., 1997; Takai et al., 2001; Kashefi and Lovley, 2003). We also Steam samples were collected over a wide geographical estimated cell concentrations and steam flow rates in area (Table 1). We evaluated the sample collector for order to gauge the dispersal potential of fumaroles. latent heat release over a 5 min period in which an 8 ml Table 1. Fumarole sampling locations and physical conditions. Location Latitude/longitude Temperature (°C) pH Type Sulphur Springs, Valles Caldera 53°54′26″ N 89 2.0 Sulfur National Reserve, New Mexico 106°36′59″ W Sulphur Works, Lassen Volcanic 40°26′60″ N 93 3.2 Sulfur National Park, California 121°32′02″ W Roaring Mountain, sulfur vent, 44°46′47″ N 87 3.01 Sulfur Yellowstone National Park (YNP), Wyoming 110°44′15″ W Roaring Mountain, origin 44°46′46″ N 93.5 0.87 Non-sulfur water sample, YNPa 110°44′19″ W Amphitheater Springs, YNP 44°48′04″ N 76 3.2 Sulfur sulfur vent 110°43′44″ W Scott’s Vent, Mutnovsky 52°28′02″ N 94 3.9 Sulfur Volcano, Kamchatka, Russia 158°09′34″E Rick’s Vent, Hawaii N/A 82 2.7 Sulfur a. Water sampled at the origin of the southern effluent of Roaring Mountain. N/A, not available. © 2008 The Authors Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 10, 1582–1590 1584 D. G. Ellis, R. W. Bizzoco and S. T. Kelley sample was condensed from steam as a control. Under ideal conditions we calculated that a mean value of 2.51 kJ g-1 was required to condense control water vapour samples. Given that the change of phase from vapour to liquid (i.e. the latent heat of vaporization- condensation of water) is 2.26 kJ g-1 at 100°C, the con- denser is reasonably effective and on average requires only an additional ~251 J release per gram control vapour sample collected. Figure 2 presents the collection rate of several sulfur and non-sulfur vent samples in the field. At Amphitheater Springs sulfur vent, samples collected on two different days showed different collection rates, likely due to a change in the volume of fumarolic steam. In contrast, there was little variability in collecting control samples on two different days. The results showed that steam sample Fig. 2. Collection rates at steam vents. Sulphur Works, Lassen collection in the field is effective despite day-to-day vari- Volcanic National Park, sulfur vent (᭜); Roaring Mountain, ability and multiple samples can be collected within a 3 h Yellowstone National Park, sulfur vent (᭿), non-sulfur vent (ᮀ); period. Amphitheater Springs, sulfur vent 5/19/2006 (᭹), 5/20/2006 (᭺); controls collected on two consecutive days ( and ᭝); Hawaii, Our portable steam collector proved extremely effective sulfur vent (¥). for capturing significant numbers of microbes from high temperature acidic fumarole steam waters in Kamchatka, Hawaii, New Mexico, California and Wyoming (Figs 3 methods, and isolate Archaea from the enrichments and and 4; Table 1). With these collections we were able to subcultures. DNA-4′,6′-diamidino-2-phenylindole (DAPI) estimate cell concentrations in fumarole steam water, staining and phase-contrast microscopy showed that extract DNA for polymerase chain reaction (PCR) cloning steam from all vents contained cells (Figs 3 and 4). Direct Fig. 3. DAPI and phase-contrast microscopy showing vent microorganisms. Cells visualized by phase contrast and by DAPI fluorescence. A. Amphitheater vent phase contrast. B. Amphitheater vent DAPI. C. Amphitheater vent enrichment phase contrast. D. Amphitheater vent enrichment DAPI. E. Amphitheater vent subculture phase contrast. F. Amphitheater vent subculture DAPI. Bar (A)–(F), 20 mm. © 2008 The Authors Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 10, 1582–1590 Archaea in fumaroles 1585 tion amplifications using ‘universal’ archaeal primers of GenomiPhi-treated DNA extractions produced bands from five of the seven fumarole steam samples and one spring water sample (Table 1). None of the GenomiPhi-treated negative DNA extraction controls (for outside air contami- nation or reagent contamination) produced PCR bands with the archaeal primers even when we extended the reactions to 35 cycles to increase detection of contaminants. These controls indicated that any Archaea identified either by cloning or by culturing were collected from geothermal steam and not from aerial or other pos- sible environmental sources. Restriction fragment length polymorphism (RFLP) analysis of the PCR clone libraries uncovered very little sequence diversity in the libraries: two to four different sequences per 96-well plate. We sequenced approximately 900 bp of each unique PCR Fig. 4. Environmental vent cell counts using DAPI. Intact cellular clone in each plate. Phylogenetic analyses of these estimates were collected by counting at least 500 cells or 100 sequences determined that the fumarole steam samples fields.
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