Probing single cells of purple sulfur bacteria with Raman spectroscopy: carotenoids and elemental sulfur

Oren, Aharon; Mana, Lily; Jehlička, Jan

doi:10.1093/femsle/fnv021

Cited by 12 publications

(10 citation statements)

References 25 publications

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“…X‐ray diffraction (XRD) analyses of S 0 globules in bacteria of the genus Thiovulum and photosynthetic sulfur bacteria suggest that they contain S 0 in liquid form (Hageage et al, 1970; Trüper & Hathaway, 1967). In contrast, laser Raman spectroscopy provides evidence that globule S 0 in filamentous bacteria from Thioploca and Beggiatoa genera (Pasteris et al, 2001), purple sulfur photosynthetic bacteria (Oren et al, 2015), deep‐sea cold seep Erythrobacter flavus (J. Zhang et al, 2020), and MTB Mbav (Eder et al, 2014) is present predominantly in a S 8 ‐ring configuration, with evidence of microcrystallinity. By using S K‐edge XAS, globule S 0 has been argued to be dominated by cyclo‐octasulfur (S 8 ) in Thioploca and Beggiatoa species, and in polymeric chains in purple sulfur bacteria (Prange et al, 1999, 2002), while S 0 stored in globules in a mesophilic purple sulfur bacterium Allochromatium vinosum and Magnetococcus marinus MC‐1 has been argued to be cyclo‐octasulfur (George et al, 2008; Pickering et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

“…X-ray diffraction (XRD) analyses of S 0 globules in bacteria of the genus Thiovulum and photosynthetic sulfur bacteria suggest that they contain S 0 in liquid form (Hageage et al, 1970;Trüper & Hathaway, 1967). In contrast, laser Raman spectroscopy provides evidence that globule S 0 in filamentous bacteria from Thioploca and Beggiatoa genera (Pasteris et al, 2001), purple sulfur photosynthetic bacteria (Oren et al, 2015), deep-sea cold seep Erythrobacter flavus (J. Zhang et al, 2020), and MTB Mbav (Eder et al, 2014) is present predominantly in a S 8 -ring configuration, with evidence of microcrystallinity.…”

Section: Nature Of Vacuoles and Sulfur Globules Within Mcasmentioning

confidence: 95%

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Magnetotaxis as an Adaptation to Enable Bacterial Shuttling of Microbial Sulfur and Sulfur Cycling Across Aquatic Oxic‐Anoxic Interfaces

Liu

Wang

et al. 2020

JGR Biogeosciences

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Magnetotactic bacteria (MTB) widely inhabit the oxic-anoxic interface (OAI) of sediments and water columns, with their motility guided by geomagnetic fields (a behavior known as magnetotaxis). Beside biomineralizing membrane-enveloped magnetite or greigite nanocrystals called magnetosomes, cells of many MTB groups contain numerous sulfur globules within their cells. Here, by combining transmission electron microscopy and synchrotron-based scanning transmission X-ray microscopy, we investigated the cellular structure and chemistry of Candidatus Magnetobacterium casensis (Mcas), a giant rod-shaped MTB from the Nitrospirae phylum. We find that nitrate-storing vacuoles and linearly polymeric sulfur globules occur exclusively within some Mcas cells along with magnetosomal magnetite. Genomic prediction indicates that Mcas cells have the potential to oxidize sulfide to sulfate (i.e., S 2− → S 0 → SO 3 2− → SO 4 2−), to reduce sulfate to sulfide (i.e., SO 4 2− → SO 3 2− → S 2−), and to reduce nitrate to NH 4 + /N 2. Together with previous environmental observations, comparative genomic analysis allows us to propose a model for Mcas involving the microbial sulfur cycle across aquatic OAIs based on magnetotaxis. Via directional movement guided by geomagnetic fields, Mcas cells shuttle either upward to upper microoxic zones for sulfur oxidation and nitrate accumulation in the OAI, or downward to deeper anoxic zones for sulfur deposition by coupling sulfide oxidation and nitrate reduction. Development of magnetotaxis makes MTB an efficient bacterial shuttle for C, N, S, and Fe across aquatic OAI environments and likely contributes significantly to their global biogeochemical cycling. It also benefits cell growth and magnetosomal magnetite formation in MTB. Plain Language Summary Microbial sulfur cycling across the oxic-anoxic interface (OAI) of sediments and the water column is an important component of the global sulfur cycle. Electrons from deeper anoxic zones are transported to microoxic/oxic surface zones, which drives biogeochemical element cycling across OAIs. Vast amounts of sulfide are produced in deeper anoxic zones. This sulfide must either be taken up there or be oxidized completely in upper microoxic/oxic zones by sulfide oxidizers via several adaption strategies. We report here a new adaptation to the microbial sulfur cycle in a giant magnetotactic bacterium, Mcas. This MTB forms intracellular sulfur globules or vacuoles (possibly storing nitrate) along with magnetosomal magnetite, and its up-and-down movement within the OAI is guided by geomagnetic fields. This adaptation is beneficial for cell growth and magnetite biomineralization in Mcas, but it also makes magnetotactic bacteria efficient bacterial shuttles for C, N, S, and Fe in aquatic OAI environments.

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Section: Discussionmentioning

confidence: 99%

Section: Nature Of Vacuoles and Sulfur Globules Within Mcasmentioning

confidence: 95%

Magnetotaxis as an Adaptation to Enable Bacterial Shuttling of Microbial Sulfur and Sulfur Cycling Across Aquatic Oxic‐Anoxic Interfaces

Liu

Wang

et al. 2020

JGR Biogeosciences

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“…Additionally, Raman mapping produces high spatial (~1 μm) and spectral resolution analyses for detailed insights on the distribution and speciation of sulfur in the sample material. Characteristic internal vibrational (molecular) spectra make S(0) particularly easy to detect and characterize with Raman scattering 9,19,21,25–27 .…”

Section: Introductionmentioning

confidence: 99%

Low frequency Raman Spectroscopy for micron-scale and in vivo characterization of elemental sulfur in microbial samples

Nims

Cron

Wetherington

et al. 2019

Sci Rep

114

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Elemental sulfur (S(0)) is an important intermediate of the sulfur cycle and is generated by chemical and biological sulfide oxidation. Raman spectromicroscopy can be applied to environmental samples for the detection of S(0), as a practical non-destructive micron-scale method for use on wet material and living cells. Technical advances in filter materials enable the acquisition of ultra-low frequency (ULF) Raman measurements in the 10–100 cm −1 range using a single-stage spectrometer. Here we demonstrate the potency of ULF Raman spectromicroscopy to harness the external vibrational modes of previously unrecognized S(0) structures present in environmental samples. We investigate the chemical and structural nature of intracellular S(0) granules stored within environmental mats of sulfur-oxidizing γ-Proteobacteria ( Thiothrix) . In vivo intracellular ULF scans indicate the presence of amorphous cyclooctasulfur (S 8 ), clarifying enduring uncertainties regarding the content of microbial sulfur storage globules. Raman scattering of extracellular sulfur clusters in Thiothrix mats furthermore reveals an unexpected abundance of metastable β-S 8 and γ-S 8 , in addition to the stable α-S 8 allotrope. We propose ULF Raman spectroscopy as a powerful method for the micron-scale determination of S(0) structure in natural and laboratory systems, with a promising potential to shine new light on environmental microbial and chemical sulfur cycling mechanisms.

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“…An important attribute of Raman spectroscopy when applied to the analysis of biomarkers is its ability to differentiate between molecular species based on intrinsic spectral signatures. Raman spectroscopy has been used to detect cellular components such as lipids, proteins, nucleotides, carbohydrates, and pigments in both algal and bacterial cells (Ermakov et al, 2005;Tuma et al, 2005;Huang et al, 2010;Wu et al, 2011;Jehlicka et al, 2013Jehlicka et al, , 2014Jehlicka et al, , 2015Oren et al, 2015;Serrano et al, 2015;Yakubovskaya et al, 2019) to profile organic and inorganic substances (De Gelder et al, 2007), and to locate the presence of specific organic compounds in heterogeneous environmental samples (Wei et al, 2015;Tan et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Investigation of Raman Spectroscopic Signatures with Multivariate Statistics: An Approach for Cataloguing Microbial Biosignatures

Dieser

Smith

et al. 2022

Astrobiology

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Spectroscopic instruments are increasingly being implemented in the search for extraterrestrial life. However, microstructural spectral analyses of alien environments could prove difficult without knowledge on the molecular identification of individual spectral signatures. To bridge this gap, we introduce unsupervised K-means clustering as a statistical approach to discern spectral patterns of biosignatures without prior knowledge of spectral regions of biomolecules. Spectral profiles of bacterial isolates from analogous polar ice sheets were measured with Raman spectroscopy. Raman analysis identified carotenoid and violacein pigments, and key cellular features including saturated and unsaturated fats, triacylglycerols, and proteins. Principal component analysis and targeted spectra integration biplot analysis revealed that the clustering of bacterial isolates was attributed to spectral biosignatures influenced by carotenoid pigments and ratio of unsaturated/saturated fat peaks. Unsupervised K-means clustering highlighted the prevalence of the corresponding spectral peaks, while subsequent supervised permutational multivariate analysis of variance provided statistical validation for spectral differences associated with the identified cellular features. Establishing a validated catalog of spectral signatures of analogous biotic and abiotic materials, in combination with targeted supervised tools could prove effective at identifying extant biosignatures.

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Probing single cells of purple sulfur bacteria with Raman spectroscopy: carotenoids and elemental sulfur

Cited by 12 publications

References 25 publications

Magnetotaxis as an Adaptation to Enable Bacterial Shuttling of Microbial Sulfur and Sulfur Cycling Across Aquatic Oxic‐Anoxic Interfaces

Magnetotaxis as an Adaptation to Enable Bacterial Shuttling of Microbial Sulfur and Sulfur Cycling Across Aquatic Oxic‐Anoxic Interfaces

Low frequency Raman Spectroscopy for micron-scale and in vivo characterization of elemental sulfur in microbial samples

Investigation of Raman Spectroscopic Signatures with Multivariate Statistics: An Approach for Cataloguing Microbial Biosignatures

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