Signature Lipids and Stable Carbon Isotope Analyses of Octopus Spring Hyperthermophilic Communities Compared with Those of Aquificales Representatives

Abstract

The molecular and isotopic compositions of lipid biomarkers of cultured Aquificales genera have been used to study the community and trophic structure of the hyperthermophilic pink streamers and vent biofilm from Octopus Spring. Thermocrinis ruber, Thermocrinis sp. strain HI 11/12, Hydrogenobacter thermophilus TK-6, Aquifex pyrophilus, and Aquifex aeolicus all contained glycerol-ether phospholipids as well as acyl glycerides. The n-C 20:1 and cy-C 21 fatty acids dominated all of the Aquificales, while the alkyl glycerol ethers were mainly C 18:0 . These Aquificales biomarkers were major constituents of the lipid extracts of two Octopus Spring samples, a biofilm associated with the siliceous vent walls, and the well-known pink streamer community (PSC). Both the biofilm and the PSC contained mono-and dialkyl glycerol ethers in which C 18 and C 20 alkyl groups were prevalent. Phospholipid fatty acids included both the Aquificales n-C 20:1 and cy-C 21 , plus a series of isobranched fatty acids (i-C 15:0 to i-C 21:0 ), indicating an additional bacterial component. Biomass and lipids from the PSC were depleted in 13 C relative to source water CO 2 by 10.9 and 17.2‰, respectively. The C 20-21 fatty acids of the PSC were less depleted than the iso-branched fatty acids, 18.4 and 22.6‰, respectively. The biomass of T. ruber grown on CO 2 was depleted in 13 C by only 3.3‰ relative to C source. In contrast, biomass was depleted by 19.7‰ when formate was the C source. Independent of carbon source, T. ruber lipids were heavier than biomass (؉1.3‰). The depletion in the C 20-21 fatty acids from the PSC indicates that Thermocrinis biomass must be similarly depleted and too light to be explained by growth on CO 2 . Accordingly, Thermocrinis in the PSC is likely to have utilized formate, presumably generated in the spring source region.Based on phylogenetic analysis of small-subunit rRNA sequences, hyperthermophilic organisms proliferate in the deepest branches of the Bacterial and Archaeal domains. The branch lengths of these hyperthermophilic lineages tend to be short, which further suggests that such organisms are the closest known extant descendants of the last common ancestor and retain many ancestral phenotypic properties (49). The recent discovery of filamentous microfossils preserved in a 3,235-million-year-old submarine volcanogenic deposit lends considerable weight to the theory that hydrothermal vent organisms have had a very long history on Earth (41). Hyperthermophilic microbes are also attracting astrobiological and biogeochemical interest because of their potential role in the formation of many kinds of mineral deposits and the generation of rock textures and mineral assemblages that may be diagnostic for extant or extinct life beyond Earth (5).A well-known example of a hyperthermophilic chemolithotrophic ecosystem is the pink filamentous streamers found at Octopus Spring in Yellowstone National Park (YNP), United States that were described by Brock in 1965 (3, 4). Similar streamer communities were first reported b...

Microbial Composition of Near-Boiling Silica-Depositing Thermal Springs throughout Yellowstone National Park

“…PCRs using archaeal primers failed to amplify, despite several attempts with various archaeon-specific primers (not shown), suggesting that Archaea are rare in these communities. Analyses of lipids in the subaqueous community of the Octopus Spring source pool show that although archaeol is present, it is in very small quantities relative to bacterial lipids (15). The abundance of bacteria in these environments is supported by DNA hybridization analyses of various springs in Yellowstone (13), and by an SSU rDNA study of Japanese alkaline springs (34).…”

“…Because many of the members of the order Aquificales are hydrogen oxidizers, it is likely that primary production in these ecosystems is driven by chemoautotrophic hydrogen oxidation. The results of a recent comparative study of the carbon isotopic signature of the Octopus Spring pink filamentous streamer community and cultured cells of Thermocrinis ruber suggest that these organisms may also be using formate as a carbon and energy source (15).…”

Biogeochemistry of intertidal microbial mats from Qatar: New insights from organic matter characterisation

“…8f). Nonisoprenoid DAGEs have been detected in hydrothermal environments Jahnke et al, 2001;Pancost et al, 2005Pancost et al, , 2006Bradley et al, 2009;Kaur et al, 2011;Hamilton-Brehm et al, 2013), upper Pliocene iron sulphide nodules (van Dongen et al, 2007), and diverse marine sediments (Hinrichs et al, 2000;Pancost et al, 2001;Blumenberg et al, 2004;Arning et al, 2008;Hernandez-Sanchez et al, 2014). Here, given that the peak concentration of DAGEs corresponded to the presence of sulphate-reducing bacteria, we suggest that these are the source, as has been inferred in settings dominated by anaerobic oxidation of methane (Hinrichs et al, 2000;Pancost et al, 2001;Blumenberg et al, 2004), and consistent with their recent identification in a mesophilic strain of Deltaproteobacteria (Grossi et al, 2015, Vinçon-Laugier et al, 2016.…”

Structural determination of the polar glycoglycerolipids from thermophilic bacteria Meiothermus taiwanensis

“…The linkages and configurations of the carbohydrate moiety were then elucidated by MS and various NMR analyses. Thus, the major glycolipid from M. taiwanensis ATCC BAA-400 was determined with the following structure:where N-acyl is C 17:0 or hydroxy C 17:0 fatty acid and the glycerol esters were mainly iso-and anteisobranched C 15:0 and C 17:0 .Keywords: glycolipid; Meiothermus taiwanensis; MS; NMR; thermophilic bacteria.The thermophilic bacteria such as Aquifex pyrophilus, Thermodesulfotobacterium commune, Thermus scotoductus, Thermomicrobium roseum and Thermodesulfatator indicus contain unique polar lipids as major membrane components [1][2][3][4][5][6][7][8]. Those lipids are essential for the thermal stability and biological functions of the bacteria in extreme environments [9][10][11].…”

“…The thermophilic bacteria such as Aquifex pyrophilus, Thermodesulfotobacterium commune, Thermus scotoductus, Thermomicrobium roseum and Thermodesulfatator indicus contain unique polar lipids as major membrane components [1][2][3][4][5][6][7][8]. Those lipids are essential for the thermal stability and biological functions of the bacteria in extreme environments [9][10][11].…”