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A 102 kb RepABC plasmid of xenologous origin modulates chromosomal gene expression in Dinoroseobacter shibae

ABSTRACT: The model organism Dinoroseobacter shibae and many other marine Rhodobacterales (Roseobacteraceae, Alphaproteobacteria) are characterized by a multipartite genome organization. Here we show that the original isolate (Dshi-6) contained six extrachromosomal replicons (ECRs), whereas the strain deposited at the DSMZ (Dshi-5) lacked a 102 kb plasmid. To determine the role of the sixth plasmid, we investigated the genomic and physiological differences between the two strains. Therefore, both genomes were (re-)sequenced and gene expression, growth and substrate utilization were examined. For comparison, we included additional plasmid-cured strains in the genome analysis. In the Dshi-6 population, the conjugative 102 kb RepABC-9 plasmid was only present in about 50 % of the cells, irrespective of its experimentally validated stability. In the presence of the sixth plasmid, copy number changes of other ECRs, in particular a decrease of the 86 kb plasmid, were observed. The most conspicuous finding was the strong influence of plasmids on the chromosomal gene expression, especially the repression of the CtrA regulon and the activation of the denitrification gene cluster. The expression is inversely controlled either by the presence of the 102 kb or the absence of the 86 kb plasmid. We identified global regulatory genes on both plasmids, i.e. a sigma 70 factor, and a quorum sensing synthase, that might be responsible for these major changes. The tremendous effects challenge the current understanding of the relevance of volatile plasmids not only for the original host, but also for new recipients after conjugation.

ORGANISM(S): Dinoroseobacter shibae

PROVIDER: GSE198318 | GEO | 2022/03/13

REPOSITORIES: GEO

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Project description:Aerobic anoxygenic phototrophic bacteria (AAPs) of the Roseobacter group are abundant in the photic zone of the marine environment. Dinoroseobacter shibae, a typical representative, converts light into additional energy that enhances its survival under nutrient-depletion. AAPs produce cytotoxic singlet oxygenunder light exposition, but D. shibae developed mechanisms to counteract the lethal effects of illumination. Recent studies documented a pivotal role of extrachromosomal elements (ECRs) for the ecological fitness of roseobacters, and here we investigated their significance for the adaptation to specific environmental stress. D. shibae possessing five ECRs, i.e. three chromids and two plasmids, was starved for four weeks in the dark and light/dark cycles and the survival strategy was evaluated using transcriptomics. Few genes on the chromosome showed differential expression between non-starved and starved cells, in particular those with a role in oxidative stress response and photosynthesis. Extrachromosomal genes in contrast showed a systematic loss of transcriptional activity, especially in the dark starved cells. The observed silencing of gene expression was not due to plasmid loss, because all five ECRs were stably maintained. Exceptionally, the smallest 72-kb replicon was the least downregulated, and one region with genes for singlet oxygen stress response was even strongly activated under light/dark cycle. A ?72-kb curing mutant completely lost the ability to benefit from AAP under starvation, and we could thus document the essential role of the 72-kb chromid to light-stress adaptation. . Our data moreover suggest that the four ECRs of D. shibae without a vital function are transcriptionally silenced under starvation. Loop-design, two biological replicates of D. shibae DFL12T cultivated in artificial salt water medium with succinate as carbon source and 12/12 light-dark cycles. After reaching stationary phase the cells were starved for 4 weeks in the dark or under light-dark cycle.

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A 102 kb RepABC plasmid of xenologous origin modulates chromosomal gene expression in Dinoroseobacter shibae

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