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Oxidative stress and starvation in Dinoroseobacter shibae: the role of extrachromosomal elements.

Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H - Front Microbiol (2015)

Bottom Line: However, light exposure results in the production of cytotoxic reactive oxygen species in AAPs.The observed decrease of gene expression was not due to plasmid loss, as all five ECRs were maintained in the cells.Interestingly, the genes on the 72-kb chromid were the least downregulated, and one region with genes of the oxygen stress response and a light-dependent protochlorophyllide reductase of cyanobacterial origin was strongly activated under the light/dark cycle.

View Article: PubMed Central - PubMed

Affiliation: Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl-von-Ossietzky University of Oldenburg Oldenburg, Germany.

ABSTRACT
Aerobic anoxygenic phototrophic bacteria (AAP) are abundant in the photic zone of the marine environment. Dinoroseobacter shibae, a representative of the Roseobacter group, converts light into additional energy that enhances its survival especially under starvation. However, light exposure results in the production of cytotoxic reactive oxygen species in AAPs. Here we investigated the response of D. shibae to starvation and oxidative stress, focusing on the role of extrachromosomal elements (ECRs). D. shibae possessing five ECRs (three plasmids and two chromids) was starved for 4 weeks either in the dark or under light/dark cycles and the survival was monitored. Transcriptomics showed that on the chromosome genes with a role in oxidative stress response and photosynthesis were differentially expressed during the light period. Most extrachromosomal genes in contrast showed a general loss of transcriptional activity, especially in dark-starved cells. The observed decrease of gene expression was not due to plasmid loss, as all five ECRs were maintained in the cells. Interestingly, the genes on the 72-kb chromid were the least downregulated, and one region with genes of the oxygen stress response and a light-dependent protochlorophyllide reductase of cyanobacterial origin was strongly activated under the light/dark cycle. A Δ72-kb curing mutant lost the ability to survive under starvation in a light/dark cycle demonstrating the essential role of this chromid for adaptation to starvation and oxidative stress. Our data moreover suggest that the other four ECRs of D. shibae have no vital function under the investigated conditions and therefore were transcriptionally silenced.

No MeSH data available.


Related in: MedlinePlus

Overview of differential gene expression of D. shibae cells starved for two days. (A) log2-fold changes in chromosomal genes; the upper box represents the light/dark cycle (LD) and the lower portray the dark (DD) starved cells. (B) The theoretical quantile-quantile (q–q) plot is shown for both LD (gray) and DD (black) chromosome genes, which are generally used to compare the distribution, showed that they are normally distributed. (C) log2-fold changes in the ECRs. The upper lane represents the q-q plot and the lower represents the gene expression pattern of the ECRs. Expression under light/dark cycling (LD) and continuous dark (DD) is shown for each gene with gray and black circles, respectively.
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Figure 3: Overview of differential gene expression of D. shibae cells starved for two days. (A) log2-fold changes in chromosomal genes; the upper box represents the light/dark cycle (LD) and the lower portray the dark (DD) starved cells. (B) The theoretical quantile-quantile (q–q) plot is shown for both LD (gray) and DD (black) chromosome genes, which are generally used to compare the distribution, showed that they are normally distributed. (C) log2-fold changes in the ECRs. The upper lane represents the q-q plot and the lower represents the gene expression pattern of the ECRs. Expression under light/dark cycling (LD) and continuous dark (DD) is shown for each gene with gray and black circles, respectively.

Mentions: The high number of extrachromosomal genes with lower expression under DD compared to NS made us wonder if there was a transcriptional repression of the ECRs or even replicon loss under this condition. Thus, we compared the changes between LD and DD versus NS for all genes separated by replicon, i.e., the chromosome and the five ECRs. Chromosomal genes displayed concurrently up- and down-regulation in both LD and DD conditions as visualized by position specific and quantile-quantile (q-q) plots comparing the actual data to a theoretical normally distributed dataset of the same range (Figures 3A,B). For the ECR genes, the q-q-plots showed that there is indeed a strong shift toward lower expression under starvation in the dark, but, although not as pronounced, also under light/dark cycles in comparison to the non-starved cells (Figure 3C). Thus, transcriptional activity of the ECRs seems to be reduced under both, LD and DD conditions.


Oxidative stress and starvation in Dinoroseobacter shibae: the role of extrachromosomal elements.

Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H - Front Microbiol (2015)

Overview of differential gene expression of D. shibae cells starved for two days. (A) log2-fold changes in chromosomal genes; the upper box represents the light/dark cycle (LD) and the lower portray the dark (DD) starved cells. (B) The theoretical quantile-quantile (q–q) plot is shown for both LD (gray) and DD (black) chromosome genes, which are generally used to compare the distribution, showed that they are normally distributed. (C) log2-fold changes in the ECRs. The upper lane represents the q-q plot and the lower represents the gene expression pattern of the ECRs. Expression under light/dark cycling (LD) and continuous dark (DD) is shown for each gene with gray and black circles, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4373377&req=5

Figure 3: Overview of differential gene expression of D. shibae cells starved for two days. (A) log2-fold changes in chromosomal genes; the upper box represents the light/dark cycle (LD) and the lower portray the dark (DD) starved cells. (B) The theoretical quantile-quantile (q–q) plot is shown for both LD (gray) and DD (black) chromosome genes, which are generally used to compare the distribution, showed that they are normally distributed. (C) log2-fold changes in the ECRs. The upper lane represents the q-q plot and the lower represents the gene expression pattern of the ECRs. Expression under light/dark cycling (LD) and continuous dark (DD) is shown for each gene with gray and black circles, respectively.
Mentions: The high number of extrachromosomal genes with lower expression under DD compared to NS made us wonder if there was a transcriptional repression of the ECRs or even replicon loss under this condition. Thus, we compared the changes between LD and DD versus NS for all genes separated by replicon, i.e., the chromosome and the five ECRs. Chromosomal genes displayed concurrently up- and down-regulation in both LD and DD conditions as visualized by position specific and quantile-quantile (q-q) plots comparing the actual data to a theoretical normally distributed dataset of the same range (Figures 3A,B). For the ECR genes, the q-q-plots showed that there is indeed a strong shift toward lower expression under starvation in the dark, but, although not as pronounced, also under light/dark cycles in comparison to the non-starved cells (Figure 3C). Thus, transcriptional activity of the ECRs seems to be reduced under both, LD and DD conditions.

Bottom Line: However, light exposure results in the production of cytotoxic reactive oxygen species in AAPs.The observed decrease of gene expression was not due to plasmid loss, as all five ECRs were maintained in the cells.Interestingly, the genes on the 72-kb chromid were the least downregulated, and one region with genes of the oxygen stress response and a light-dependent protochlorophyllide reductase of cyanobacterial origin was strongly activated under the light/dark cycle.

View Article: PubMed Central - PubMed

Affiliation: Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl-von-Ossietzky University of Oldenburg Oldenburg, Germany.

ABSTRACT
Aerobic anoxygenic phototrophic bacteria (AAP) are abundant in the photic zone of the marine environment. Dinoroseobacter shibae, a representative of the Roseobacter group, converts light into additional energy that enhances its survival especially under starvation. However, light exposure results in the production of cytotoxic reactive oxygen species in AAPs. Here we investigated the response of D. shibae to starvation and oxidative stress, focusing on the role of extrachromosomal elements (ECRs). D. shibae possessing five ECRs (three plasmids and two chromids) was starved for 4 weeks either in the dark or under light/dark cycles and the survival was monitored. Transcriptomics showed that on the chromosome genes with a role in oxidative stress response and photosynthesis were differentially expressed during the light period. Most extrachromosomal genes in contrast showed a general loss of transcriptional activity, especially in dark-starved cells. The observed decrease of gene expression was not due to plasmid loss, as all five ECRs were maintained in the cells. Interestingly, the genes on the 72-kb chromid were the least downregulated, and one region with genes of the oxygen stress response and a light-dependent protochlorophyllide reductase of cyanobacterial origin was strongly activated under the light/dark cycle. A Δ72-kb curing mutant lost the ability to survive under starvation in a light/dark cycle demonstrating the essential role of this chromid for adaptation to starvation and oxidative stress. Our data moreover suggest that the other four ECRs of D. shibae have no vital function under the investigated conditions and therefore were transcriptionally silenced.

No MeSH data available.


Related in: MedlinePlus