scholarly journals The Proximity of Ribosomal Protein Genes tooriCEnhancesVibrio choleraeFitness in the Absence of Multifork Replication

mBio ◽  
2017 ◽  
Vol 8 (1) ◽  
Author(s):  
Alfonso Soler-Bistué ◽  
Michaël Timmermans ◽  
Didier Mazel
Keyword(s):  
Life Cycle ◽  
Ribosomal Protein ◽  
Gene Order ◽  
Growth Conditions ◽  
Fast Growth ◽  
Optimization Strategy ◽  
Ribosomal Protein Genes ◽  
Fast Growing ◽  
Growth Optimization ◽  
Whole Life Cycle

ABSTRACTRecent works suggest that bacterial gene order links chromosome structure to cell homeostasis. Comparative genomics showed that, in fast-growing bacteria, ribosomal protein genes (RP) locate near the replication origin (oriC). We recently showed thatVibrio choleraeemploys this positional bias as a growth optimization strategy: under fast-growth conditions, multifork replication increases RP dosage and expression. However, RP location may provide advantages in a dosage-independent manner: for example, the physical proximity of the many ribosomal components, in the context of a crowded cytoplasm, may favor ribosome biogenesis. To uncover putative dosage-independent effects, we studied isogenicV. choleraederivatives in which the major RP locus,S10-spc-α(S10), was relocated to alternative genomic positions. When bacteria grew fast, bacterial fitness was reduced according to the S10 relative distance tooriC. The growth of wild-typeV. choleraecould not be improved by additional copies of the locus, suggesting a physiologically optimized genomic location. Slow growth is expected to uncouple RP position from dosage, since multifork replication does not occur. Under these conditions, we detected a fitness impairment when S10 was far fromoriC. Deep sequencing followed by marker frequency analysis in the absence of multifork replication revealed an up to 30% S10 dosage reduction associated with its relocation that closely correlated with fitness alterations. Hence, the impact of S10 location goes beyond a growth optimization strategy during feast periods. RP location may be important during the whole life cycle of this pathogen.IMPORTANCEThe role of gene order within the bacterial chromosome is poorly understood. In fast growers, the location of genes linked with the expression of genetic information (i.e., transcription and translation) is biased towardoriC. It was proposed that the location of these genes helps to maximize their expression by recruiting multifork replication during fast growth. Our results show that such genomic positioning impacts cell fitness beyond fast-growth conditions, probably across the whole life cycle of fast growers. Thus, the genomic position of key highly expressed genes, such as RP, was finely tuned during the evolution of fast-growing bacteria and may also be important in slow growers. In the near future, many more genes whose genomic position impacts bacterial phenotype will be described. These studies will contribute to discovery the rules of genome organization and application of them for the design of synthetic chromosomes and the creation of artificial life forms.

scholarly journals Vibrionaceae core, shell and cloud genes are non-randomly distributed on Chr 1: An hypothesis that links the genomic location of genes with their intracellular placement

BMC Genomics ◽  
2020 ◽  
Vol 21 (1) ◽  
Author(s):  
Cecilie Bækkedal Sonnenberg ◽  
Tim Kahlke ◽  
Peik Haugen
Keyword(s):  
Gene Expression ◽  
Expression Patterns ◽  
Fast Growth ◽  
Gene Copy ◽  
Distribution Data ◽  
Optimization Strategy ◽  
Gene Distribution ◽  
Fast Growing ◽  
Genomic Location ◽  
Growing Conditions

Abstract Background The genome of Vibrionaceae bacteria, which consists of two circular chromosomes, is replicated in a highly ordered fashion. In fast-growing bacteria, multifork replication results in higher gene copy numbers and increased expression of genes located close to the origin of replication of Chr 1 (ori1). This is believed to be a growth optimization strategy to satisfy the high demand of essential growth factors during fast growth. The relationship between ori1-proximate growth-related genes and gene expression during fast growth has been investigated by many researchers. However, it remains unclear which other gene categories that are present close to ori1 and if expression of all ori1-proximate genes is increased during fast growth, or if expression is selectively elevated for certain gene categories. Results We calculated the pangenome of all complete genomes from the Vibrionaceae family and mapped the four pangene categories, core, softcore, shell and cloud, to their chromosomal positions. This revealed that core and softcore genes were found heavily biased towards ori1, while shell genes were overrepresented at the opposite part of Chr 1 (i.e., close to ter1). RNA-seq of Aliivibrio salmonicida and Vibrio natriegens showed global gene expression patterns that consistently correlated with chromosomal distance to ori1. Despite a biased gene distribution pattern, all pangene categories contributed to a skewed expression pattern at fast-growing conditions, whereas at slow-growing conditions, softcore, shell and cloud genes were responsible for elevated expression. Conclusion The pangene categories were non-randomly organized on Chr 1, with an overrepresentation of core and softcore genes around ori1, and overrepresentation of shell and cloud genes around ter1. Furthermore, we mapped our gene distribution data on to the intracellular positioning of chromatin described for V. cholerae, and found that core/softcore and shell/cloud genes appear enriched at two spatially separated intracellular regions. Based on these observations, we hypothesize that there is a link between the genomic location of genes and their cellular placement.

scholarly journals Differential expression of duplicated ribosomal protein genes modifies ribosome composition in response to stress

2019 ◽  
Vol 48 (4) ◽  
pp. 1954-1968 ◽  
Author(s):  
Mustafa Malik Ghulam ◽  
Mathieu Catala ◽  
Sherif Abou Elela
Keyword(s):  
Ribosomal Protein ◽  
Rna Polymerase Ii ◽  
Ribosomal Proteins ◽  
Normal Growth ◽  
Growth Conditions ◽  
Duplicated Genes ◽  
Ribosomal Protein Genes ◽  
Expression Ratio ◽  
Gene Copies ◽  
Response To Stress

Abstract In Saccharomyces cerevisiae, most ribosomal proteins are synthesized from duplicated genes, increasing the potential for ribosome heterogeneity. However, the contribution of these duplicated genes to ribosome production and the mechanism determining their relative expression remain unclear. Here we demonstrate that in most cases, one of the two gene copies generate the bulk of the active ribosomes under normal growth conditions, while the other copy is favored only under stress. To understand the origin of these differences in paralog expression and their contribution to ribosome heterogeneity we used RNA polymerase II ChIP-Seq, RNA-seq, polyribosome association and peptide-based mass-spectrometry to compare their transcription potential, splicing, mRNA abundance, translation potential, protein abundance and incorporation into ribosomes. In normal conditions a post-transcriptional expression hierarchy of the duplicated ribosomal protein genes is the product of the efficient splicing, high stability and efficient translation of the major paralog mRNA. Exposure of the cell to stress modifies the expression ratio of the paralogs by repressing the expression of the major paralog and thus increasing the number of ribosomes carrying the minor paralog. Together the data indicate that duplicated ribosomal protein genes underlie a modular network permitting the modification of ribosome composition in response to changing growth conditions.

scholarly journals Vibrionaceae core, shell and cloud genes are non-randomly distributed on Chr 1: An hypothesis that links the genomic location of genes with their intracellular placement

2020 ◽  
Author(s):  
Cecilie Bækkedal Sonnenberg ◽  
Tim Kahlke ◽  
Peik Haugen
Keyword(s):  
Gene Expression ◽  
Expression Patterns ◽  
Fast Growth ◽  
Gene Copy ◽  
Distribution Data ◽  
Optimization Strategy ◽  
Gene Distribution ◽  
Fast Growing ◽  
Genomic Location ◽  
Growing Conditions

Abstract Background: The genome of Vibrionaceae bacteria, which consists of two circular chromosomes, is replicated in a highly ordered fashion. In fast-growing bacteria, multifork replication results in higher gene copy numbers and increased expression of genes located close to the origin of replication of Chr 1 (ori1). This is believed to be a growth optimization strategy to satisfy the high demand of essential growth factors during fast growth. The relationship between ori1-proximate growth-related genes and gene expression during fast growth has been investigated by many researchers. However, it remains unclear which other gene categories that are present close to ori1 and if expression of all ori1-proximate genes is increased during fast growth, or if expression is selectively elevated for certain gene categories.Results: We calculated the pangenome of all complete genomes from the Vibrionaceae family and mapped the four pangene categories, core, softcore, shell and cloud, to their chromosomal positions. This revealed that core and softcore genes were found heavily biased towards ori1, while shell genes were overrepresented at the opposite part of Chr 1 (i.e., close to ter1). RNA-seq of Aliivibrio salmonicida and Vibrio natriegens showed global gene expression patterns that consistently correlated with chromosomal distance to ori1. Despite a biased gene distribution pattern, all pangene categories contributed to a skewed expression pattern at fast-growing conditions, whereas at slow-growing conditions, softcore, shell and cloud genes were responsible for elevated expression.Conclusion: The pangene categories were non-randomly organized on Chr 1, with an overrepresentation of core and softcore genes around ori1, and overrepresentation of shell and cloud genes around ter1. Furthermore, we mapped our gene distribution data on to the intracellular positioning of chromatin described for V. cholerae, and found that core/softcore and shell/cloud genes appear enriched at two spatially separated intracellular regions. Based on these observations, we hypothesize that there is a link between the genomic location of genes and their cellular placement.

scholarly journals Vibrionaceae core and shell genes are non-randomly distributed into spatially distinct intracellular domains

2020 ◽  
Author(s):  
Cecilie Sonnenberg Bækkedal ◽  
Tim Kahlke ◽  
Peik Haugen
Keyword(s):  
Gene Expression ◽  
Expression Patterns ◽  
Global Gene Expression ◽  
Fast Growth ◽  
Gene Copy ◽  
Distribution Data ◽  
Optimization Strategy ◽  
Gene Distribution ◽  
Fast Growing ◽  
Growing Conditions

Abstract Background: The genome of Vibrionaceae bacteria, which consists of two circular chromosomes, is replicated in a highly ordered fashion. In fast-growing bacteria, multifork replication results in higher gene copy numbers and increased expression of genes located close to the origin of replication of Chr 1 (ori1 ). This is believed to be a growth optimization strategy to satisfy the high demand of essential growth factors during fast growth. The relationship between ori1 -proximate growth-related genes and gene expression during fast growth has been investigated by many researchers. However, it remains unclear which other gene categories that are present close to ori1 and if expression of all ori1 -proximate genes is increased during fast growth, or if expression is selectively elevated for certain gene categories. Results: We calculated the pangenome of all complete genomes from the Vibrionaceae family and mapped the four pangene categories, core, softcore, shell and cloud, to their chromosomal positions. This revealed that core and softcore genes were found heavily biased towards ori1 , while shell genes were overrepresented at the opposite part of Chr 1 (i.e., close to ter1 ). RNA-seq of Aliivibrio salmonicida and Vibrio natriegens showed global gene expression patterns that consistently correlated with chromosomal distance to ori1 . Despite a biased gene distribution pattern, all pangene categories contributed to a skewed expression pattern at fast-growing conditions, whereas at slow-growing conditions, softcore, shell and cloud genes were responsible for elevated expression. Conclusion: The pangene categories were non-randomly organized on the two chromosomes, with an overrepresentation of core and softcore genes around ori1 . We mapped our gene distribution data on to the intracellular positioning of chromatin described for V. cholerae , and suggested that core/softcore and shell/cloud genes were enriched at two spatially separated intracellular regions in the cell. The concurrence of the spatial distribution of core and the level of gene expression in one intracellular region, implied that there is a link between the structural organization of core genes and their cellular function in the cell.

scholarly journals Vibrionaceae core, shell and cloud genes are non-randomly distributed on Chr 1: An hypothesis that links the genomic location of genes with their intracellular placement

2020 ◽  
Author(s):  
Cecilie Bækkedal Sonnenberg ◽  
Tim Kahlke ◽  
Peik Haugen
Keyword(s):  
Gene Expression ◽  
Expression Patterns ◽  
Fast Growth ◽  
Gene Copy ◽  
Distribution Data ◽  
Optimization Strategy ◽  
Gene Distribution ◽  
Fast Growing ◽  
Genomic Location ◽  
Growing Conditions

Abstract Background: The genome of Vibrionaceae bacteria, which consists of two circular chromosomes, is replicated in a highly ordered fashion. In fast-growing bacteria, multifork replication results in higher gene copy numbers and increased expression of genes located close to the origin of replication of Chr 1 (ori1). This is believed to be a growth optimization strategy to satisfy the high demand of essential growth factors during fast growth. The relationship between ori1-proximate growth-related genes and gene expression during fast growth has been investigated by many researchers. However, it remains unclear which other gene categories that are present close to ori1 and if expression of all ori1-proximate genes is increased during fast growth, or if expression is selectively elevated for certain gene categories.Results: We calculated the pangenome of all complete genomes from the Vibrionaceae family and mapped the four pangene categories, core, softcore, shell and cloud, to their chromosomal positions. This revealed that core and softcore genes were found heavily biased towards ori1, while shell genes were overrepresented at the opposite part of Chr 1 (i.e., close to ter1). RNA-seq of Aliivibrio salmonicida and Vibrio natriegens showed global gene expression patterns that consistently correlated with chromosomal distance to ori1. Despite a biased gene distribution pattern, all pangene categories contributed to a skewed expression pattern at fast-growing conditions, whereas at slow-growing conditions, softcore, shell and cloud genes were responsible for elevated expression.Conclusion: The pangene categories were non-randomly organized on Chr 1, with an overrepresentation of core and softcore genes around ori1, and overrepresentation of shell and cloud genes around ter1. Furthermore, we mapped our gene distribution data on to the intracellular positioning of chromatin described for V. cholerae, and found that core/softcore and shell/cloud genes appear enriched at two spatially separated intracellular regions. Based on these observations, we hypothesize that there is a link between the genomic location of genes and their cellular placement.

scholarly journals Mechanisms coordinating ribosomal protein gene transcription in response to stress

2020 ◽  
Vol 48 (20) ◽  
pp. 11408-11420 ◽  
Author(s):  
Sevil Zencir ◽  
Daniel Dilg ◽  
Maria Paula Rueda ◽  
David Shore ◽  
Benjamin Albert
Keyword(s):  
Ribosomal Protein ◽  
Protein Gene ◽  
Ribosomal Protein Gene ◽  
Growth Conditions ◽  
Binding Property ◽  
Protein Homeostasis ◽  
Ribosomal Protein Genes ◽  
Core Set ◽  
Response To Stress ◽  
Maximal Expression

Abstract While expression of ribosomal protein genes (RPGs) in the budding yeast has been extensively studied, a longstanding enigma persists regarding their co-regulation under fluctuating growth conditions. Most RPG promoters display one of two distinct arrangements of a core set of transcription factors (TFs) and are further differentiated by the presence or absence of the HMGB protein Hmo1. However, a third group of promoters appears not to be bound by any of these proteins, raising the question of how the whole suite of genes is co-regulated. We demonstrate here that all RPGs are regulated by two distinct, but complementary mechanisms driven by the TFs Ifh1 and Sfp1, both of which are required for maximal expression in optimal conditions and coordinated downregulation upon stress. At the majority of RPG promoters, Ifh1-dependent regulation predominates, whereas Sfp1 plays the major role at all other genes. We also uncovered an unexpected protein homeostasis-dependent binding property of Hmo1 at RPG promoters. Finally, we show that the Ifh1 paralog Crf1, previously described as a transcriptional repressor, can act as a constitutive RPG activator. Our study provides a more complete picture of RPG regulation and may serve as a paradigm for unravelling RPG regulation in multicellular eukaryotes.

Sign in / Sign up

Export Citation Format

Share Document