Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Eddie, Brian J.; Hanson, Thomas E.

doi:10.1128/jb.01342-12

Cited by 21 publications

(49 citation statements)

References 57 publications

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“…Enhanced glycogen storage on sulfide suggests that C. tepidum may use glycogen synthesis in part to cope with and/or store excess reducing power available during sulfide oxidation. This is consistent with the induction of a high-velocity, low-affinity sulfide: quinone oxidoreductase (CT1087) whose physiological role seems to be primarily sulfide tolerance (51,64,65).…”

Section: Discussionsupporting

confidence: 56%

Chlorobaculum tepidum Modulates Amino Acid Composition in Response to Energy Availability, as Revealed by a Systematic Exploration of the Energy Landscape of Phototrophic Sulfur Oxidation

Levy

Lee

Hanson

2016

Appl Environ Microbiol

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Microbial sulfur metabolism, particularly the formation and consumption of insoluble elemental sulfur (S 0 ), is an important biogeochemical engine that has been harnessed for applications ranging from bioleaching and biomining to remediation of waste streams. Chlorobaculum tepidum, a low-light-adapted photoautolithotrophic sulfur-oxidizing bacterium, oxidizes multiple sulfur species and displays a preference for more reduced electron donors: sulfide > S 0 > thiosulfate. To understand this preference in the context of light energy availability, an "energy landscape" of phototrophic sulfur oxidation was constructed by varying electron donor identity, light flux, and culture duration. Biomass and cellular parameters of C. tepidum cultures grown across this landscape were analyzed. From these data, a correction factor for colorimetric protein assays was developed, enabling more accurate biomass measurements for C. tepidum, as well as other organisms. C. tepidum's bulk amino acid composition correlated with energy landscape parameters, including a tendency toward less energetically expensive amino acids under reduced light flux. This correlation, paired with an observation of increased cell size and storage carbon production under electron-rich growth conditions, suggests that C. tepidum has evolved to cope with changing energy availability by tuning its proteome for energetic efficiency and storing compounds for leaner times. IMPORTANCEHow microbes cope with and adapt to varying energy availability is an important factor in understanding microbial ecology and in designing efficient biotechnological processes. We explored the response of a model phototrophic organism, Chlorobaculum tepidum, across a factorial experimental design that enabled simultaneous variation and analysis of multiple growth conditions, what we term the "energy landscape." C. tepidum biomass composition shifted toward less energetically expensive amino acids at low light levels. This observation provides experimental evidence for evolved efficiencies in microbial proteomes and emphasizes the role that energy flux may play in the adaptive responses of organisms. From a practical standpoint, our data suggest that bulk biomass amino acid composition could provide a simple proxy to monitor and identify energy stress in microbial systems. Microbes that synthesize or degrade insoluble sulfur minerals are instrumental in the biogeochemical sulfur cycle (1) and have been applied for biomining (2, 3) and sulfide remediation (4-7). However, little is known about how these organisms respond to fluctuations in available energy due to shifts in electron donor identity, fixed carbon availability, or light in the case of phototrophic bacteria. A deeper understanding of microbial strategies for coping with energy fluctuations has the potential to improve microbe-catalyzed industrial processes (8) and to impact our understanding of microbial ecology as shaped by energy availability (9). Furthermore, a specific understanding of these adaptations among mic...

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Section: Discussionsupporting

confidence: 56%

Chlorobaculum tepidum Modulates Amino Acid Composition in Response to Energy Availability, as Revealed by a Systematic Exploration of the Energy Landscape of Phototrophic Sulfur Oxidation

Levy

Lee

Hanson

2016

Appl Environ Microbiol

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“…For CT1276, a similar response on sulfide was reported recently (50). The adjacent gene, CT1277, exhibited a strong increase in the relative transcription level on sulfide as well, and for this gene's product, a role in sulfide-dependent gene expression changes was suggested, based on its DNA-binding domain (50). The corresponding gene in A. vinosum is encoded by Alvin_1742, which is located adjacent but transcribed in the opposite direction to the gene cluster of A. vinosum.…”

Section: Resultsmentioning

confidence: 49%

“…BLAST searches for Alvin_1737 and Alvin_1740 revealed similarities to CT1276 of Chlorobaculum tepidum TLS. For CT1276, a similar response on sulfide was reported recently (50). The adjacent gene, CT1277, exhibited a strong increase in the relative transcription level on sulfide as well, and for this gene's product, a role in sulfide-dependent gene expression changes was suggested, based on its DNA-binding domain (50).…”

Section: Resultsmentioning

confidence: 74%

“…SreABC has been shown to reduce not only elemental sulfur but also polysulfides in vitro (49). For A. vinosum, the respective gene products could in principle be involved in the oxidation of the polysulfides that occur as intermediates during the oxidation of sulfide to sulfur that is stored in sulfur globules, just as has been speculated for the related proteins from Chlorobaculum tepidum (50). In both cases, the iron-sulfur cluster-containing ␤-subunit as well as the active site molybdopterin-containing ␣-subunit is predicted to be oriented toward the bacterial periplasm.…”

Section: Resultsmentioning

confidence: 99%

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Genome-Wide Transcriptional Profiling of the Purple Sulfur Bacterium Allochromatium vinosum DSM 180T during Growth on Different Reduced Sulfur Compounds

Weißgerber

Dobler

Polen

et al. 2013

Journal of Bacteriology

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bThe purple sulfur bacterium Allochromatium vinosum DSM 180 T is one of the best-studied sulfur-oxidizing anoxygenic phototrophic bacteria, and it has been developed into a model organism for laboratory-based studies of oxidative sulfur metabolism. Here, we took advantage of the organism's high metabolic versatility and performed whole-genome transcriptional profiling to investigate the response of A. vinosum cells upon exposure to sulfide, thiosulfate, elemental sulfur, or sulfite compared to photoorganoheterotrophic growth on malate. Differential expression of 1,178 genes was observed, corresponding to 30% of the A. vinosum genome. Relative transcription of 551 genes increased significantly during growth on one of the different sulfur sources, while the relative transcript abundance of 627 genes decreased. A significant number of genes that revealed strongly enhanced relative transcription levels have documented sulfur metabolism-related functions. Among these are the dsr genes, including dsrAB for dissimilatory sulfite reductase, and the sgp genes for the proteins of the sulfur globule envelope, thus confirming former results. In addition, we identified new genes encoding proteins with appropriate subcellular localization and properties to participate in oxidative dissimilatory sulfur metabolism. Those four genes for hypothetical proteins that exhibited the strongest increases of mRNA levels on sulfide and elemental sulfur, respectively, were chosen for inactivation and phenotypic analyses of the respective mutant strains. This approach verified the importance of the encoded proteins for sulfur globule formation during the oxidation of sulfide and thiosulfate and thereby also documented the suitability of comparative transcriptomics for the identification of new sulfur-related genes in anoxygenic phototrophic sulfur bacteria.

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“…Significantly increased relative mRNA levels for the genes Alvin_1317-Alvin_1319, encoding the three subunits of a putative sulfur or polysulfide reductase with highest similarities to archaeal SreABC (55), led us to propose that the purple sulfur bacterial protein may be involved in the transformation of polysulfides to stored sulfur (13). A similar function was proposed for the related proteins from Chlorobaculum tepidum (56) and is further supported by the elevated protein levels for Alvin_1317, Alvin_1318, and Alvin_1319 detected during sulfide oxidation (Tables 1 and 3).…”

Section: Resultsmentioning

confidence: 91%

A Comparative Quantitative Proteomic Study Identifies New Proteins Relevant for Sulfur Oxidation in the Purple Sulfur Bacterium Allochromatium vinosum

Weißgerber

Sylvester

Kröninger

et al. 2014

Appl Environ Microbiol

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bIn the present study, we compared the proteome response of Allochromatium vinosum when growing photoautotrophically in the presence of sulfide, thiosulfate, and elemental sulfur with the proteome response when the organism was growing photoheterotrophically on malate. Applying tandem mass tag analysis as well as two-dimensional (2D) PAGE, we detected 1,955 of the 3,302 predicted proteins by identification of at least two peptides (59.2%) and quantified 1,848 of the identified proteins. Altered relative protein amounts (>1.5-fold) were observed for 385 proteins, corresponding to 20.8% of the quantified A. vinosum proteome. A significant number of the proteins exhibiting strongly enhanced relative protein levels in the presence of reduced sulfur compounds are well documented essential players during oxidative sulfur metabolism, e.g., the dissimilatory sulfite reductase DsrAB. Changes in protein levels generally matched those observed for the respective relative mRNA levels in a previous study and allowed identification of new genes/proteins participating in oxidative sulfur metabolism. One gene cluster (hyd; Alvin_2036-Alvin_2040) and one hypothetical protein (Alvin_2107) exhibiting strong responses on both the transcriptome and proteome levels were chosen for gene inactivation and phenotypic analyses of the respective mutant strains, which verified the importance of the so-called Isp hydrogenase supercomplex for efficient oxidation of sulfide and a crucial role of Alvin_2107 for the oxidation of sulfur stored in sulfur globules to sulfite. In addition, we analyzed the sulfur globule proteome and identified a new sulfur globule protein (SgpD; Alvin_2515).

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Chlorobaculum tepidum TLS Displays a Complex Transcriptional Response to Sulfide Addition

Cited by 21 publications

References 57 publications

Chlorobaculum tepidum Modulates Amino Acid Composition in Response to Energy Availability, as Revealed by a Systematic Exploration of the Energy Landscape of Phototrophic Sulfur Oxidation

Chlorobaculum tepidum Modulates Amino Acid Composition in Response to Energy Availability, as Revealed by a Systematic Exploration of the Energy Landscape of Phototrophic Sulfur Oxidation

Genome-Wide Transcriptional Profiling of the Purple Sulfur Bacterium Allochromatium vinosum DSM 180T during Growth on Different Reduced Sulfur Compounds

A Comparative Quantitative Proteomic Study Identifies New Proteins Relevant for Sulfur Oxidation in the Purple Sulfur Bacterium Allochromatium vinosum

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