Lipid Biomolecules in Silica Sinters: Indicators of Microbial Biodiversity

Blackwell Science, LtdOxford, UKEMIEnvironmental Microbiology1462-2912Society for Applied Microbiology and Blackwell Publishing Ltd, 2004716677Original ArticleLipid biomarkers in silica sintersR. D. Pancost et al . Environmental Microbiology (2005) 7(1), 66–77 doi:10.1111/j.1462-2920.2004.00686.x Lipid biomolecules in silica sinters: indicators of microbial biodiversity Richard D. Pancost,1* Sarah Pressley,1 ceous sinters is of broad scientific interest. From their 16S Joanna M. Coleman,1 Liane G. Benning2 and rRNA, many geothermal organisms appear to be quite B. W. Mountain3 primitive such that insight into their diversity and ecology 1Organic Geochemistry Unit, Bristol Biogeochemistry is a critical component of origin of life studies and, poten- Research Centre, School of Chemistry, University of tially, astrobiology (Stetter, 1996). In addition, siliceous Bristol, Cantock’s Close, Bristol BS8 1TS, UK. sinters are of economic interest as they commonly host 2School of Earth Sciences, University of Leeds, Leeds epithermal gold and silver deposits (Jones et al., 2001a). LS2 9JT, UK. Finely laminated siliceous sinters are built up from 3Institute of Geological and Nuclear Sciences, Wairakei amorphous silica masses that precipitate during cooling Research Centre, Private Bag 2000, Taupo, New Zealand. of hydrothermal fluids that are supersaturated with silica (e.g. Konhauser et al., 2001; Mountain et al., 2003). In the Summary past 20 years, a variety of thermophiles and hyperthermo- philes has been found in such settings, occurring as mats, To explore further the diversity of the microorganisms in hydrothermal fluids and on the surfaces of and and their relationship with geothermal sinters, we entrained in mineral deposits. These microorganisms can examined the lipids preserved in six sinters associ- be highly abundant and could play an important role in ated with four different hot spring (58–82∞C) areas of sinter formation. Association of microorganisms with sili- the Taupo Volcanic Zone (TVZ), New Zealand. These ceous sinters has been reported from a range of hot sinters contain microbial remains, but the process of springs in Yellowstone National Park, USA, the Kenyan mineralization has rendered them largely unidentifi- Rift Valley and the Taupo Volcanic Zone in New Zealand able. Dominant lipids include free fatty acids, 1,2- (Jones et al., 1996; 1998; 2001b; Renaut et al., 1996; diacylglycerophospholipids, 1,2-di-O-alkylglycerols, Mountain et al., 2003). glycerol dialkylglycerol tetraethers and 1-O- The Taupo Volcanic Zone (TVZ; Fig. 1) is situated cen- alkylglycerols. These confirm the presence and, in trally on the North Island of New Zealand. The area is some cases, high abundances of bacteria in all six 300 km long and up to 60 km wide, as defined by vent sinters and archaea in four of the six sinter samples; positions and caldera structures, from Mount Ruapehu to in addition, the presence of novel macrocyclic White Island, both active volcanoes. The area is the most diethers and unusual distributions of monoethers and frequently active and productive silicic volcanic system on diethers suggest the presence of previously unchar- Earth, and available data suggest that this has been the acterized bacteria. The lipid distributions are also case for at least the past 0.34 million years (Wilson et al., markedly dissimilar among the four sites; for exam- 1995). Associated with this volcanism are several high- ple, novel macrocyclic diethers are restricted to the temperature (>250∞C) geothermal systems through which Rotokawa samples while particularly abundant mono- a natural heat output of ª 4200 MW is channelled (Bibby ethers occur only in the Orakei Korako sample. Thus, et al., 1995). Steam and gas escaping from these deep biomarkers can provide crucial insight into the com- hot-water systems appears at the surface as fumarolic plex community structure of thermophilic microor- activity or may be absorbed by superficial groundwaters ganisms, including both archaea and bacteria, to form distinctive hot spring systems (Henley and Ellis, involved with biogenic silica sinter formation. 1983; Fig. 2). Although their presence has now been confirmed, it is Introduction difficult to elucidate the role and nature of microorganisms The study of microbial biomineralization in geothermal related to siliceous sinter precipitation because progres- systems and their particular role in the formation of sili- sive silicification can destroy cytoplasmic details and wall structure making it difficult to identify biosilicified organisms on morphological grounds (Jones et al., 1996; 1997). Received 1 April, 2004; revised 15 June, 2004; accepted 15 June, 2004. *For correspondence. E-mail [email protected]; Tel. Thus, although the presence of biomineralized microor- (+44) 117 974 4540; Fax (+44) 117 929 3746. ganisms has been confirmed in a large variety of modern © 2004 Society for Applied Microbiology and Blackwell Publishing Ltd Lipid biomarkers in silica sinters 67 Phospholipid fatty acids The abundances of the fatty acids released from saponi- fication of the polar fraction, and thus inferred to derive from hydrolysis of 1,2 diacylglycerophospholipids (III, Fig. 3; phospholipid fatty acids, PLFAs), are highly variable with total abundances varying by nearly an order of magnitude among the studied samples (Table 1; representative chromatograms shown in Fig. 4). Inferred PLFA distributions are similarly variable as reflected by large differences in the average chain length and the ratio of unsaturated to saturated components. The Rotokawa samples, characterized by high temperature and low pH, contain very simple fatty acid distributions in the post- hydrolysis polar fractions. Specifically, fatty acids are characterized predominantly by saturated and straight-chain C16 and C18 components, an absence of branched components and relatively low ratios of unsaturated to saturated PLFAs. This suggests that the fatty acids derive from sources other than bacteria, possibly higher plant debris, and are not present as PLFAs, which appear not to have been well preserved. This is unsurprising considering the high temperatures of these springs, 80–82∞C. The free Fig. 1. Map of the North Island of New Zealand, showing the Taupo acid fraction does contain much higher abundances of Volcanic Zone and location of hydrothermal springs (white and black circles); those shown in white are the sites investigated in this study. fatty acids (data not shown), consistent with this explana- tion; however, the free fatty acids have a distribution similar to that expected for higher plant material, and clear sinters, it can be difficult to determine which organisms evidence for an abundance of bacterial 1,2 diacylglycero- were present during sinter formation. Particularly prob- phospholipids (relative to other compounds, described lematic has been the identification of Archaea in sinters below) is weak. and any assessment of their role in silicification (Renaut The samples from the other sites contain more abun- and Jones, 2000). Biomarkers (Fig. 3) can be used in the dant inferred PLFAs with more complex distributions. The identification of microorganisms. Such efforts have been Orakei Korako sample contains high abundances of pre- applied to cold seep authigenic carbonates (Thiel et al., dominantly C and C PLFAs, but the unsaturated com- 2001; Aloisi et al., 2002), while in hydrothermal settings, 16 18 ponents are of equal or greater abundance than their studies have mainly concerned the mat-building organ- saturated equivalents. C and C components are simi- isms (Dobson et al., 1988; Robinson and Eglinton, 1990; 16 18 larly abundant in the Waiotapu silicate, but also present Zeng et al., 1992a,b; van der Meer et al., 2000; Jahnke are high quantities of C unsaturated and saturated et al., 2004). Here, we report biomarker distributions and 20 PLFAs, distinguishing it from all other samples. Both Wair- abundances for six amorphous silica sinters from four akei sinters contain very high abundances of C and C different areas of the TVZ (Fig. 2). These are used to 16 18 saturated PLFAs while unsaturated C components, characterize microbial diversity and assess the relative 18 branched (iso and anteiso) and cyclopropyl-bearing C abundances of different microorganisms (e.g. bacteria 16 components and branched (iso and anteiso) C compo- versus archaea) in siliceous sinter deposits. 17 nents are also present, all occurring in similar distributions in both samples. Results Biomarker distributions are heterogeneous among the six Non-isoprenoidal ether lipids samples examined. The most abundant compounds in these samples are free fatty acids, 1,2 diacylglycerophos- The abundances of ether lipids composed of non- pholipids [analysed as fatty acid methyl esters (FAMEs) isoprenoidal alkyl moieties (i.e. either straight chain or after base hydrolysis; Fig. 4] and a variety of neutral ether bearing a single methyl substituent) are quite variable lipids (Fig. 5), including 1,2-di-O-alkylglycerols (diethers), (representative chromatograms shown in Fig. 5; Table 2). glycerol dialkylglycerol tetraethers (GDGTs) and 1-O- 1-O-alkylglycerols (monoethers) are highly heteroge- alkylglycerols (monoethers). neous in their occurrence, being present in only trace © 2004 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 7, 66–77 68 R. D. Pancost et al. A C B D Fig. 2. Photos of sample sites described in this paper. A. Wastewater drain at the Wairakei Power Station showing subaqueous, fan-like growths of silica sinter (sample site WR-1, T = 65∞C, pH 8.5). The top of the photo is bounded by the subaerial top of the concrete divider. Water flows from right to left at ª0.3 m s-1. Field of view is 1 m in width. B. South-east margin of the main upflow at Rotokawa (sample site RK-1F, T = 82∞C, pH 3.8). Margin of pool is surrounded by spicular microstromatolites composed of amorphous silica. C. North-east margin of Champagne Pool, Waiotapu (sample site WT-1, T = 75∞C, pH 5.5). Subaqueous domal stromatolites are on the left. A rim of native sulfur lies at the air–water interface.

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