DOE PAGES Journal Article: Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum
Title: Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum
ImagesFigures / Tables (8)
Elemental sulfur (S0) is produced and degraded by phylogenetically diverse groups of microorganisms. For Chlorobaculum tepidum, an anoxygenic phototroph, sulfide is oxidized to produce extracellular S0 globules, which can be further oxidized to sulfate. While some sulfur-oxidizing bacteria (e.g., Allochromatium vinosum) are also capable of growth on commercial S0 as an electron donor, C. tepidum is not. Even colloidal sulfur sols, which appear indistinguishable from biogenic globules, do not support the growth of C. tepidum. Here, we investigate the properties that make biogenic S0 globules distinct from abiotic forms of S0. We found that S0 globules produced by C. tepidum and abiotic S0 sols are quite similar in terms of mineralogy and material properties, but the two are distinguished primarily by the properties of their surfaces. C. tepidum's globules are enveloped by a layer of organics (protein and polysaccharides), which results in a surface that is fundamentally different from that of abiotic S0 sols. The organic coating on the globules appears to slow the aging and crystallization of amorphous sulfur, perhaps providing an extended window of time for microbes in the environment to access the more labile forms of sulfur as needed. Overall, our results suggest that the surface ofmore » biogenic S0 globules may be key to cell–sulfur interactions and the reactivity of biogenic S0 in the environment.« less
Marnocha, Cassandra L. [1]; Sabanayagam, Chandran R. [2]; Modla, Shannon [2]; Powell, Deborah H. [2]; Henri, Pauline A. [3]; Steele, Andrew S. [4]; Hanson, Thomas E. [5]; Webb, Samuel M. [6]; Chan, Clara S. [5]
Niagara Univ., Lewiston, NY (United States); Univ. of Delaware, Newark, DE (United States)
Delaware Biotechnology Inst., Newark, DE (United States)
Univ. of Delaware, Newark, DE (United States)
Carnegie Inst. of Science, Washington, DC (United States)
Delaware Biotechnology Inst., Newark, DE (United States); Univ. of Delaware, Newark, DE (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
AC02-76SF00515; INBRE220RR016472-09; MCB-1244373; EPS-0814251
Journal Volume: 10; Journal ID: ISSN 1664-302X
Frontiers Research Foundation
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; elemental sulfur; biomineralization; sulfur cycling; green sulfur bacteria; microbe-mineral interactions
Marnocha, Cassandra L., Sabanayagam, Chandran R., Modla, Shannon, Powell, Deborah H., Henri, Pauline A., Steele, Andrew S., Hanson, Thomas E., Webb, Samuel M., and Chan, Clara S. Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum. United States: N. p., 2019. Web. doi:10.3389/fmicb.2019.00271.
Marnocha, Cassandra L., Sabanayagam, Chandran R., Modla, Shannon, Powell, Deborah H., Henri, Pauline A., Steele, Andrew S., Hanson, Thomas E., Webb, Samuel M., & Chan, Clara S. Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum. United States. https://doi.org/10.3389/fmicb.2019.00271
Marnocha, Cassandra L., Sabanayagam, Chandran R., Modla, Shannon, Powell, Deborah H., Henri, Pauline A., Steele, Andrew S., Hanson, Thomas E., Webb, Samuel M., and Chan, Clara S. Mon . "Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum". United States. https://doi.org/10.3389/fmicb.2019.00271. https://www.osti.gov/servlets/purl/1506230.
title = {Insights Into the Mineralogy and Surface Chemistry of Extracellular Biogenic S0 Globules Produced by Chlorobaculum tepidum},
author = {Marnocha, Cassandra L. and Sabanayagam, Chandran R. and Modla, Shannon and Powell, Deborah H. and Henri, Pauline A. and Steele, Andrew S. and Hanson, Thomas E. and Webb, Samuel M. and Chan, Clara S.},
abstractNote = {Elemental sulfur (S0) is produced and degraded by phylogenetically diverse groups of microorganisms. For Chlorobaculum tepidum, an anoxygenic phototroph, sulfide is oxidized to produce extracellular S0 globules, which can be further oxidized to sulfate. While some sulfur-oxidizing bacteria (e.g., Allochromatium vinosum) are also capable of growth on commercial S0 as an electron donor, C. tepidum is not. Even colloidal sulfur sols, which appear indistinguishable from biogenic globules, do not support the growth of C. tepidum. Here, we investigate the properties that make biogenic S0 globules distinct from abiotic forms of S0. We found that S0 globules produced by C. tepidum and abiotic S0 sols are quite similar in terms of mineralogy and material properties, but the two are distinguished primarily by the properties of their surfaces. C. tepidum's globules are enveloped by a layer of organics (protein and polysaccharides), which results in a surface that is fundamentally different from that of abiotic S0 sols. The organic coating on the globules appears to slow the aging and crystallization of amorphous sulfur, perhaps providing an extended window of time for microbes in the environment to access the more labile forms of sulfur as needed. Overall, our results suggest that the surface of biogenic S0 globules may be key to cell–sulfur interactions and the reactivity of biogenic S0 in the environment.},
doi = {10.3389/fmicb.2019.00271},
journal = {Frontiers in Microbiology},
https://doi.org/10.3389/fmicb.2019.00271
Figures / Tables:
Figure 1: Chlorobaculum tepidum biogenic S0 globules (Ct S0) compared to a standard of bulk crystalline $\alpha$-S8. (A) XRD patterns, with peak broadening in S0 globules. (B) Raman spectra.
All figures and tables (8 total)
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Ultrafast Spectroscopic Investigation of Energy Transfer in Site-Directed Mutants of the Fenna–Matthews–Olson (FMO) Antenna Complex from Chlorobaculum tepidum
Journal Article Magdaong, Nikki Cecil M. ; Saer, Rafael G. ; Niedzwiedzki, Dariusz M. ; ... - Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
Ultrafast transient absorption (TA) and time-resolved fluorescence (TRF) spectroscopic studies were performed on several mutants of the bacteriochlorophyll (BChl) a-containing Fenna–Matthews–Olson (FMO) complex from the green sulfur bacterium Chlorobaculum tepidum. These mutants were generated to perturb a particular BChl a site and determine its effects on the optical spectroscopic properties of the pigment–protein complex. Measurements conducted at 77 K under both oxidizing and reducing conditions revealed changes in the dynamics of the various spectral components as compared to the data set from wild-type FMO. TRF results show that under reducing conditions all FMO samples decay with a similar lifetime inmore » the ~2 ns range. The oxidized samples revealed varying fluorescence lifetimes of the terminal BChl a emitter, considerably shorter than those recorded for the reduced samples, indicating that the quenching mechanism in wild-type FMO is still present in the mutants. Global fitting of TA data yielded similar overall results, and in addition, the lifetimes of early decaying components were determined. Target analyses of TA data for select FMO samples generated kinetic models that better simulate the TA data. Here, a comparison of the lifetime of excitonic components for all samples reveals that the mutations affect mainly the early kinetic components, but not that of the lowest energy exciton, which reflects the flexibility of energy transfer in FMO.« less
https://doi.org/10.1021/acs.jpcb.7b01270
Effect of Spectral Density Shapes on the Excitonic Structure and Dynamics of the Fenna–Matthews–Olson Trimer from Chlorobaculum tepidum
Journal Article Kell, Adam ; Blankenship, Robert E. ; Jankowiak, Ryszard - Journal of Physical Chemistry. A, Molecules, Spectroscopy, Kinetics, Environment, and General Theory
The Fenna–Matthews–Olson (FMO) trimer (composed of identical subunits) from the green sulfur bacterium Chlorobaculum tepidum is an important protein model system to study exciton dynamics and excitation energy transfer (EET) in photosynthetic complexes. In addition, FMO is a popular model for excitonic calculations, with many theoretical parameter sets reported describing different linear and nonlinear optical spectra. Due to fast exciton relaxation within each subunit, intermonomer EET results predominantly from the lowest energy exciton states (contributed to by BChl α 3 and 4). Using experimentally determined shapes for the spectral densities, simulated optical spectra are obtained for the entire FMO trimer.more » Simultaneous fits of low-temperature absorption, fluorescence, and hole-burned spectra place constraints on the determined pigment site energies, providing a new Hamiltonian that should be further tested to improve modeling of 2D electronic spectroscopy data and our understanding of coherent and dissipation effects in this important protein complex.« less
https://doi.org/10.1021/acs.jpca.6b03107
X-ray absorption spectroscopy of bacterial sulfur globules
Journal Article George, Graham N - Microbiology
Sulfur K-edge X-ray absorption spectroscopy is a powerful in situ probe of sulfur biochemistry in intact cells and tissues. Under favorable circumstances the technique can provide quantitative information on the chemical identify of the sulfur species that are present in a sample. Prange et al. have recently reported an X-ray absorption spectroscopic study of bacterial sulfur storage globules. Unfortunately there are substantial problems with the experimental technique employed that, they contend, lead to completely erroneous conclusions. In the more recent of their two papers Prange et al. employed a curve-fitting method similar to that used by us (for more thanmore » 10 years). In essence, the method employs simply fitting a linear combination of the spectra of standard compounds to that of the unknown, in this case cultures of bacterial cells. This type of analysis can provide quantitative estimates of the individual sulfur types in the sample, but is critically dependent upon the choice of reference spectra. Prange et al. deduce substantial differences between the chemical forms of sulfur stored in the globules of different organisms; they conclude that the globules of Beggiatoa alba and Thiomargarita namibiensis contain cyclo-octasulfur (S{sub 8}), while those of other organisms contain polythionates (Acidithiobacillus ferrooxidans) and polymeric sulfur (e.g. Allochromatium vinosum). This is in contradiction with an earlier study, in which they found that sulfur in all globule species examined resembled that expected for various sized spherical particles of S{sub 8}. The discrepancy is due to an experimental artefact in the work of Prange et al. arising from their choice of transmittance detection, which is also discussed.« less
https://doi.org/10.1099/00221287-148-8-2267
Journal Article George, G N ; Gnida, M ; Bazylinski, D A ; ... - J. Bacteriol. 190:6376,2008
The chemical nature of the sulfur in bacterial sulfur globules has been the subject of controversy for a number of years. Sulfur K-edge X-ray absorption spectroscopy (XAS) is a powerful technique for probing the chemical forms of sulfur in situ, but two groups have used it with very different conclusions. The root of the controversy lies with the different detection strategies used by the two groups, which result in very different spectra. This paper seeks to resolve the controversy. We experimentally demonstrate that the use of transmittance detection for sulfur K-edge XAS measurements is highly prone to spectroscopic distortions andmore » that much of the published work on sulfur bacteria is very likely based on distorted data. We also demonstrate that all three detection methods used for X-ray absorption experiments yield essentially identical spectra when the measurements are carried out under conditions where no experimental distortions are expected. Finally, we turn to the original question--the chemical nature of bacterial sulfur. We examine isolated sulfur globules of Allochromatium vinosum and intact cells of a strain of magnetotactic coccus and show that XAS indicates the presence of a chemical form of sulfur resembling S{sub 8}.« less
Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS
Journal Article Mehta-Kolte, Misha G. ; Loutey, Dana ; Wang, Ouwei ; ... - mBio (Online)
The genetic and biochemical basis of perchlorate-dependent H2S oxidation (PSOX) was investigated in the dissimilatory perchlorate-reducing microorganism (DPRM)Azospira suillumPS (PS). Previously, it was shown that all known DPRMs innately oxidize H2S, producing elemental sulfur (So). Although the process involving PSOX is thermodynamically favorable (ΔG°' = -206 kJ ∙ mol-1H2S), the underlying biochemical and genetic mechanisms are currently unknown. Interestingly, H2S is preferentially utilized over physiological electron donors such as lactate or acetate although no growth benefit is obtained from the metabolism. Here, we determined that PSOX is due to a combination of enzymatic and abiotic interactions involving reactive intermediates of perchlorate respiration.more » Using various approaches, including barcode analysis by sequencing (Bar-seq), transcriptome sequencing (RNA-seq), and proteomics, along with targeted mutagenesis and biochemical characterization, we identified all facets of PSOX in PS. In support of our proposed model, deletion of identified upregulated PS genes traditionally known to be involved in sulfur redox cycling (e.g., Sox, sulfide:quinone reductase [SQR]) showed no defect in PSOX activity. Proteomic analysis revealed differential abundances of a variety of stress response metal efflux pumps and divalent heavy-metal transporter proteins, suggesting a general toxicity response. Furthermore,in vitrobiochemical studies demonstrated direct PSOX mediated by purified perchlorate reductase (PcrAB) in the absence of other electron transfer proteins. The results of these studies support a model in which H2S oxidation is mediated by electron transport chain short-circuiting in the periplasmic space where the PcrAB directly oxidizes H2S to So. The biogenically formed reactive intermediates (ClO2-and O2) subsequently react with additional H2S, producing polysulfide and Soas end products.IMPORTANCEInorganic sulfur compounds are widespread in nature, and microorganisms are central to their transformation, thereby playing a key role in the global sulfur cycle. Sulfur oxidation is mediated by a broad phylogenetic diversity of microorganisms, including anoxygenic phototrophs and either aerobic or anaerobic chemotrophs coupled to oxygen or nitrate respiration, respectively. Recently, perchlorate-respiring microorganisms were demonstrated to be innately capable of sulfur oxidation regardless of their phylogenetic affiliation. As recognition of the prevalence of these organisms intensifies, their role in global geochemical cycles is being queried. This is further highlighted by the recently recognized environmental pervasiveness of perchlorate not only across Earth but also throughout our solar system. The inferred importance of this metabolism not only is that it is a novel and previously unrecognized component of the global sulfur redox cycle but also is because of the recently demonstrated applicability of perchlorate respiration in the control of biogenic sulfide production in engineered environments such as oil reservoirs and wastewater treatment facilities, where excess H2S represents a significant environmental, process, and health risk, with associated costs approximating $90 billion annually.IMPORTANCEInorganic sulfur compounds are widespread in nature, and microorganisms are central to their transformation, thereby playing a key role in the global sulfur cycle. Sulfur oxidation is mediated by a broad phylogenetic diversity of microorganisms, including anoxygenic phototrophs and either aerobic or anaerobic chemotrophs coupled to oxygen or nitrate respiration, respectively. Recently, perchlorate-respiring microorganisms were demonstrated to be innately capable of sulfur oxidation regardless of their phylogenetic affiliation. As recognition of the prevalence of these organisms intensifies, their role in global geochemical cycles is being queried. This is further highlighted by the recently recognized environmental pervasiveness of perchlorate not only across Earth but also throughout our solar system. The inferred importance of this metabolism not only is that it is a novel and previously unrecognized component of the global sulfur redox cycle but also is because of the recently demonstrated applicability of perchlorate respiration in the control of biogenic sulfide production in engineered environments such as oil reservoirs and wastewater treatment facilities, where excess H2S represents a significant environmental, process, and health risk, with associated costs approximating $90 billion annually.« less
https://doi.org/10.1128/mbio.02023-16