Insights into chemotaxonomic composition and carbon cycling of phototrophic communities in an artesian sulfur-rich spring (Zodletone, Oklahoma, USA), a possible analog for ancient microbial mat systems

Department of Geosciences, Universität Bremen, Bremen, Germany.
Geobiology (Impact Factor: 3.83). 03/2011; 9(2):166-79. DOI: 10.1111/j.1472-4669.2010.00268.x
Source: PubMed


Zodletone spring in Oklahoma is a unique environment with high concentrations of dissolved-sulfide (10 mm) and short-chain gaseous alkanes, exhibiting characteristics that are reminiscent of conditions that are thought to have existed in Earth's history, in particular the late Archean and early-to-mid Proterozoic. Here, we present a process-oriented investigation of the microbial community in two distinct mat formations at the spring source, (1) the top of the sediment in the source pool and (2) the purple streamers attached to the side walls. We applied a combination of pigment and lipid biomarker analyses, while functional activities were investigated in terms of oxygen production (microsensor analysis) and carbon utilization ((13)C incorporation experiments). Pigment analysis showed cyanobacterial pigments, in addition to pigments from purple sulfur bacteria (PSB), green sulfur bacteria (GSB) and Chloroflexus-like bacteria (CLB). Analysis of intact polar lipids (IPLs) in the source sediment confirmed the presence of phototrophic organisms via diacylglycerol phospholipids and betaine lipids, whereas glyceroldialkylglyceroltetraether additionally indicated the presence of archaea. No archaeal IPLs were found in the purple streamers, which were strongly dominated by betaine lipids. (13)C-bicarbonate- and -acetate-labeling experiments indicated cyanobacteria as predominant phototrophs in the source sediment, carbon was actively fixed by PSB/CLB/GSB in purple streamers by using near infrared light. Despite the presence of cyanobacteria, no oxygen could be detected in the presence of light, suggesting anoxygenic photosynthesis as the major metabolic process at this site. Our investigations furthermore indicated photoheterotrophy as an important process in both habitats. We obtained insights into a syntrophically operating phototrophic community in an ecosystem that bears resemblance to early Earth conditions, where cyanobacteria constitute an important contributor to carbon fixation despite the presence of high sulfide concentrations.

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Available from: Solveig Irena Bühring, Sep 09, 2014
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    • "While small numbers of green sulfur bacteria (GSB) are also present in and below the chemocline, the total sulfide oxidation rate cannot be attributed to PSB and GSB alone (Overmann et al., 1996a). Chemoautotrophic sulfide oxidation has been observed near the oxic–anoxic interfaces of other stratified systems and by analogy may be expected in Mahoney Lake (Hadas et al., 2001; B€ uhring et al., 2011). Analysis of 16S rRNA gene sequences supports this, showing the presence of Epsilonproteobacteria that are likely to be sulfide and/or sulfur oxidizers (Klepac-Ceraj et al., 2012). "
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    Full-text · Article · Jun 2014 · Geobiology
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    • "Previous work has documented additional non-planktonic GSB sources of isorenieratene and chlorobactene, including microbial mats (e.g. Wahlund et al., 1991; Brocks and Summons, 2003; Beatty et al., 2005; Bühring et al., 2011). Although a mixed planktonic and mat origin of the carotenoids cannot be ruled out, it is more likely that the GSB and PSB carotenoids detected in Hawsker Bottoms samples share a source. "
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    ABSTRACT: A comprehensive organic geochemical investigation of the Hawsker Bottoms outcrop section in Yorkshire, England has provided new insights about environmental conditions leading into and during the Toarcian oceanic anoxic event (T-OAE; ∼183 Ma). Rock-Eval and molecular analyses demonstrate that the section is uniformly within the early oil window. Hydrogen index (HI), organic petrography, polycyclic aromatic hydrocarbon (PAH) distributions, and tricyclic terpane ratios mark a shift to a lower relative abundance of terrigenous organic matter supplied to the sampling locality during the onset of the T-OAE and across a lithological transition. Unlike other ancient intervals of anoxia and extinction, biomarker indices of planktonic community structure do not display major changes or anomalous values. Depositional environment and redox indicators support a shift towards more reducing conditions in the sediment porewaters and the development of a seasonally stratified water column during the T-OAE. In addition to carotenoid biomarkers for green sulfur bacteria (GSB), we report the first occurrence of okenane, a marker of purple sulfur bacteria (PSB), in marine samples younger than ∼1.64 Ga. Based on modern observations, a planktonic source of okenane’s precursor, okenone, would require extremely shallow photic zone euxinia (PZE) and a highly restricted depositional environment. However, due to coastal vertical mixing, the lack of planktonic okenone production in modern marine sulfidic environments, and building evidence of okenone production in mat-dwelling Chromatiaceae, we propose a sedimentary source of okenone as an alternative. Lastly, we report the first parallel compound-specific δ13C record in marine- and terrestrial-derived biomarkers across the T-OAE. The δ13C records of short-chain n-alkanes, acyclic isoprenoids, and long-chain n-alkanes all encode negative carbon isotope excursions (CIEs), and together, they support an injection of isotopically light carbon that impacted both the atmospheric and marine carbon reservoirs. To date, molecular δ13C records of the T-OAE display a negative CIE that is smaller in magnitude compared to the bulk organic δ13C excursion. Although multiple mechanisms could explain this observation, our molecular, petrographic, and Rock-Eval data suggest that variable mixing of terrigenous and marine organic matter is an important factor affecting the bulk organic δ13C records of the T-OAE.
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    ABSTRACT: The adaptation of pyrosequencing technologies for use in culture-independent diversity surveys allowed for deeper sampling of ecosystems of interest. One extremely well suited area of interest for pyrosequencing-based diversity surveys that has received surprisingly little attention so far, is examining fine scale (e.g. micrometer to millimeter) beta diversity in complex microbial ecosystems. We examined the patterns of fine scale Beta diversity in four adjacent sediment samples (1mm apart) from the source of an anaerobic sulfide and sulfur rich spring (Zodletone spring) in southwestern Oklahoma, USA. Using pyrosequencing, a total of 292,130 16S rRNA gene sequences were obtained. The beta diversity patterns within the four datasets were examined using various qualitative and quantitative similarity indices. Low levels of Beta diversity (high similarity indices) were observed between the four samples at the phylum-level. However, at a putative species (OTU(0.03)) level, higher levels of beta diversity (lower similarity indices) were observed. Further examination of beta diversity patterns within dominant and rare members of the community indicated that at the putative species level, beta diversity is much higher within rare members of the community. Finally, sub-classification of rare members of Zodletone spring community based on patterns of novelty and uniqueness, and further examination of fine scale beta diversity of each of these subgroups indicated that members of the community that are unique, but non novel showed the highest beta diversity within these subgroups of the rare biosphere. The results demonstrate the occurrence of high inter-sample diversity within seemingly identical samples from a complex habitat. We reason that such unexpected diversity should be taken into consideration when exploring gamma diversity of various ecosystems, as well as planning for sequencing-intensive metagenomic surveys of highly complex ecosystems.
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