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Sphingomonas wittichii strain RW1 genome-wide gene expression shifts in response to dioxins and clay

ABSTRACT: Sphingomonas wittichii strain RW1 (RW1) is one of few strains that can grow on dibenzo-p-dioxin (DD). We conducted a transcriptomic study of RW1 using RNA-Seq to outline transcriptional responses to DD, dibenzofuran (DF), and the smectite clay mineral saponite (SAP), an important geosorbent of toxicants in soil, with succinate as carbon source. The ability to grow on DD is rare compared to growth on the chemically similar DF even though the same initial dioxygenase may be involved in oxidation of both substrates. Therefore we hypothesized the reason for this lies beyond catabolic pathways and may concern genes involved in processes for cell-substrate interactions such as substrate recognition and transport, and detoxification. Compared to succinate (SUC) as control carbon source, DF caused over 240 protein-coding genes to be differentially expressed, whereas more than 300 were differentially expressed with DD. Stress response genes were up-regulated by both DD and DF. This effect was stronger with DD than DF, suggesting a higher toxicity of DD compared to DF. Both DD and DF caused changes in expression of genes involved in active cross-membrane transport such as TonB dependent receptor proteins, but the patterns of changes differed between the two substrates. Multiple transcription factor genes also displayed expression patterns distinct to DD and DF growth. DD and DF induced the catechol ortho- and the salicylate/gentisate pathways, respectively. Both DD and DF induced the shared down-stream aliphatic intermediate compound pathway. Clay (SAP) caused category-wide down-regulation of genes for cell motility and chemotaxis, particularly those involved in the synthesis, assembly and functioning of flagella. This is environmentally important finding because clay is a major component of soil microbes’ microenvironment influencing local chemistry and may serve as geosorbent for toxic pollutants. Similar to clay, DD and DF also affect motility and chemotaxis.

ORGANISM(S): Rhizorhabdus wittichii

PROVIDER: GSE74831 | GEO | 2015/11/13

SECONDARY ACCESSION(S): PRJNA301621

REPOSITORIES: GEO

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Project description:Spingomonas wittichii strain RW1 can completely oxidize dibenzo-p-dioxins and dibenzofurans, which are persistent contaminants of soils and sediments. For successful application in soil bioremediation systems, strain RW1 must cope with fluctuations in water availability, or water potential. The objectives of this study were to characterize how strain RW1 responses to changes in different components of the total water potential (solute and matric potential) and to then connect these responses to more realistic scenarios of soil desiccation. To accomplish this task, transcriptome profiling was used to investigate the effects of decreasing the solute potential with sodium chloride (solute stress), decreasing the matric potential with high-molecular weight polyethylene glycol (matric stress), or inoculating cells directly into unsaturated sand (sand desiccation stress). Transcriptome profiling revealed a general response to solute, matric, and sand desiccation stress that involved synthesizing trehalose and modifying the composition of exopolysaccarides. Transcriptome profiling also revealed responses that were unique to each stress. Only solute and matric stress triggered the down-regulation of flagella genes. Only solute and sand desiccation stress triggered the up-regulation of two RNA polymerase ECF-type sigma factors along with several membrane proteins, mechanosensitive channels, and solute transporters. Finally, only matric stress triggered the up-regulation of the RNA polymerase sigma-32 factor along with several molecular chaperones. Together, this study revealed a general response to solute, matric and sand desiccation stress but also unique responses to only a subset of these stresses, suggesting that each stress affects strain RW1 in a fundamentally different way. Comparative transcriptome profiling was performed to assess the effects of acute (30 min) solute and matric stress (3 samples for acute solute stress, 3 samples for acute matric stress, 3 controls), the effects of chronic (24 hours) solute and matric stress (3 samples for chronic solute stress, 3 samples for chronic matric stress, 3 controls), and the effects of sand desiccation stress (4 samples for sand desiccation treatment, 3 controls).

Project description:The efficacy of inoculation of single pure bacterial cultures into complex microbiomes, for example, in order to achieve increased pollutant degradation rates in contaminated material (i.e., bioaugmentation), has been frustrated by insufficient knowledge on the behaviour of the inoculated bacteria under the specific abiotic and biotic boundary conditions. Here we present a comprehensive analysis of global gene expression of the bacterium Sphingomonas wittichii RW1 in contaminated sand, compared to regular suspended batch growth in liquid culture. RW1 is a well-known bacterium capable of mineralizing polycyclic aromatic hydrocarbons such as dioxins, dibenzofurans and other chlorinated congeners. We tested the reactions of the cells both during the immediate transition phase from liquid culture to sand with or without dibenzofuran, as well during growth and stationary phase in sand. Cells during transition resemble going through stationary phase, showing evidence of stress responses and nutrient scavenging, and even of major adjustments in their primary metabolism if they were not pre-cultured on the same contaminant as found in the soil. Cells growing and surviving in soil show very different signatures as in liquid or in liquid culture exposed to chemicals inducing drought stress, and we obtain evidence for numerous soil-specific expressed genes. We conclude that studies focusing on inoculation efficacy should test behavior under conditions as closely as possible mimicking the intended microbiome conditions. We were interested to study the global reactions of bacteria with biodegradative properties under near-environmental as compared to laboratory culture conditions. We compared here the genome-wide responses of RW1 between regular laboratory batch growth on the aromatic substrates DBF and salicylate with growth in sandy soil with or without the same aromatic compounds. We analysed the cellular reactions immediately after introduction into the sand, during exponential growth and at stationary phase, all in carefully controlled and replicated experimental conditions.

Project description:The efficacy of inoculation of single pure bacterial cultures into complex microbiomes, for example, in order to achieve increased pollutant degradation rates in contaminated material (i.e., bioaugmentation), has been frustrated by insufficient knowledge on the behaviour of the inoculated bacteria under the specific abiotic and biotic boundary conditions. Here we present a comprehensive analysis of global gene expression of the bacterium Sphingomonas wittichii RW1 in contaminated sand, compared to regular suspended batch growth in liquid culture. RW1 is a well-known bacterium capable of mineralizing polycyclic aromatic hydrocarbons such as dioxins, dibenzofurans and other chlorinated congeners. We tested the reactions of the cells both during the immediate transition phase from liquid culture to sand with or without dibenzofuran, as well during growth and stationary phase in sand. Cells during transition resemble going through stationary phase, showing evidence of stress responses and nutrient scavenging, and even of major adjustments in their primary metabolism if they were not pre-cultured on the same contaminant as found in the soil. Cells growing and surviving in soil show very different signatures as in liquid or in liquid culture exposed to chemicals inducing drought stress, and we obtain evidence for numerous soil-specific expressed genes. We conclude that studies focusing on inoculation efficacy should test behavior under conditions as closely as possible mimicking the intended microbiome conditions We were interested to study the global reactions of bacteria with biodegradative properties under near-environmental as compared to laboratory culture conditions. we compared here the genome-wide responses of RW1 between regular laboratory batch growth on the aromatic substrates DBF and salicylate with growth in sandy soil with or without the same aromatic compounds. We analysed the cellular reactions immediately after introduction into the sand, during lag phase, all in carefully controlled and replicated experimental conditions.

Project description:It has long been recognized that species occupy a specific ecological niche within their ecosystem. The ecological niche is defined as the number of conditions and resources that limit species distribution. Within their ecological niche, species do not exist in a single physiological state but in a number of states we call the Natural Operating Range. In this paper we link ecological niche theory to physiological ecology by measuring gene expression levels of collembolans exposed to various natural conditions. The soil-dwelling collembolan Folsomia candida was exposed to 26 natural soils with different soil characteristics (soil type, land use, practice, etc). The animals were exposed for two days and gene expression levels were measured. The main factor found to regulate gene expression was the soil type (sand or clay), in which 18.5% of the measured genes were differentially expressed. Gene Ontology analysis showed animals exposed to sandy soils experience general stress, affecting cell homeostasis and replication. Multivariate analysis linking soil chemical data to gene expression data revealed that soil fertility influences gene expression. Land-use and practice had less influence on gene expression; only forest soils showed a different expression pattern. A variation in gene expression variation analysis showed overall low variance in gene expression. The large difference in response to soil type was caused by the soil physicochemical properties where F. candida experiences clay soils and sandy soils as very different from each other. This collembolan prefers fertile soils with high organic matter content, as soil fertility was found to correlate with gene expression and animals exposed to sandy soils (which, in general, have lower organic matter content) experience more general stress. Finally, we conclude that there is no such thing as a fixed physiological state for animals in their ecological niche and the boundary between the ecological niche and a stressed state depends on the genes/pathways investigated.

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Sphingomonas wittichii strain RW1 genome-wide gene expression shifts in response to dioxins and clay

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