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

- 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.
- 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 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).
- 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.
- Full list of author information is available at the end of the article.
- cholerae, replication of Chr 1 and Chr 2 is highly coordinated [10].
- 200 kbp) between the crtS replication and the initiation of Chr 2 replication..
- The exact function of this pause is yet unknown, but it is hypothesized to be needed for activation of the rctB (Chr 2’s own replication initiator) and ori2 initiation sys- tem [12].
- In other words, the chromosomal position of crtS and the pause contribute to synchronize termin- ation of Chr 1 and Chr 2 replication.
- (2020) showed that relocation of the s10-spec-α locus lead to higher cytoplasm fluidity and the authors suggested that changes in the macromolecu- lar crowding of the cytoplasm impacts the cellular physi- ology of V.
- cholerae was independent of the position of the s10-spec-α locus [20]..
- Here, genes located on Chr 1 were 3.6 × more expressed compared to those located on Chr 2, and the highest ex- pression values were typically associated with genes sur- rounding the origin of replication on Chr 1..
- In fast-growing bac- teria, replication results in higher gene copy numbers, and increased expression of genes located close to the origin of replication of Chr 1.
- In a pangenome approach we used available genomes to calculate and divide clusters of orthologous genes into the main categories “core”, “softcore”, “shell” (accessory) and “cloud” (unique), and used this information to de- termine how the corresponding genes are distributed on Chr 1 and Chr 2 of selected Vibrionaceae genomes.
- Finally, based on our data we propose an hypothesis that de- scribes how pangenes are spatially distributed inside Vibrionaceae bacterial cells, and we discuss possible im- plications of the proposed hypothesis..
- The remaining clusters are dis- tributed among softcore (encoded by ≥ 117 genomes), shell (encoded by 116 ≤ and ≥ 3 genomes) and cloud (encoded by ≤ 2 genomes), and contain and 45,074 clusters, which represents 3, 23 and 73% of the total clusters, respectively.
- In individual genomes, core gene clusters represent 1.2% of the pangenome, and comprise 10 — 17% of the total genes.
- Similarly, softcore constitutes genes per genome) of the total genes..
- Core and softcore genes densely populate the upper half of Chr 1.
- First, genes of eleven selected Vibrionaceae representatives (see Add- itional file 2 for phylogeny of the 11 genomes) were clas- sified as either upper or lower (i.e., upper or lower half of the chromosome) based on their chromosomal loca- tion on Chr 1 and Chr 2 in relation to their distance of the origin of replication.
- ≤0.05) in the upper half of Chr 1 in all investigated ge- nomes.
- Similarly, shell and cloud genes on Chr 1 are sig- nificantly overrepresented (adjusted chi-square P-value.
- ≤0.05) in the lower half of Chr 1 in 8 genomes, thus sup- porting a non-random distribution of genes on Chr 1.
- In contrast to Chr 1, genes of all categories are much more evenly distributed on Chr 2.
- Although shell, cloud and softcore genes show non-random distribution on Chr 2 in some of the investigated genomes (softcore 3/11, shell 1/11, cloud 2/11), the majority of genomes show no sig- nificant bias (adjusted chi-square P-value ≤0.05).
- Fur- thermore, core genes were not significantly overrepresented in either lower or upper half of Chr 2 in any of the genomes..
- To provide a more fine-grained picture of the core (710—721) and shell gene distributions, we plotted the distribution of core and shell genes on Chr 1 and Chr 2 of eleven Vibrionaceae taxa using the genome comparison tool Circos [24] (Fig.
- Interestingly, although core genes densely populate the upper half of Chr 1, the region im- mediately surrounding ori1 contains very few core genes..
- In summary, the results presented here reveal that core, softcore, shell and cloud genes are non-randomly distributed on Chr 1.
- genes are more likely to be located on the upper half of Chr 1, whereas shell and cloud genes tend to be located closer to the replication terminator.
- For Chr 2, the dis- tribution of the four pangene categories are in general randomly distributed showing locational bias only for a few genomes..
- Expression levels of genes located on Chr 1 of.
- Figure 3 shows how core, softcore, shell and cloud pan- genes are distributed on Chr 1 and Chr 2 of V.
- 1 Distribution of the four pangene categories between upper and lower half of 11 Vibrionaceae genomes.
- Core and softcore genes are overrepresented on the upper half of Chr 1, shell and cloud genes are overrepresented on the lower half.
- On Chr 2 the genes are more evenly distributed between the upper and lower halves of Chr 2.
- Location of core (a) and shell (a) genes on Chr 1 and Chr 2 of 11 Vibrionaceae genomes.
- Circular plots are arranged regarding the phylogenetic relationship of the investigated isolates.
- Each plot is centered at a gene assumed to be close to the replication origin: mioC on Chr 1 and rtcB on Chr 2.
- As shown, a majority of core genes on Chr 1 is located closer to ori1 than to ter.
- Shell genes show the opposite distribution pattern on Chr 1, where majority of shell genes accumulate closer to ter.
- On Chr 2 both core and shell genes are randomly distributed.
- The dashed line “ i ” indicates a region on Chr 1 surrounding ori1 that contains very few core genes.
- The dashed line “ ii ” shows a region on Chr 1 of approximately 500 kb surrounding ter that is more sparsely populated with core genes than the rest of the chromosome.
- the biased gene distribution pattern described above, with core and softcore genes being overrepresented at the upper half of Chr 1, and shell and cloud genes being overrepresented at the lower half.
- cholerae, which showed that growth rates have large impacts on the copy number (gene dosage) of genes located on Chr 1, as well as on gene expression levels .
- 3 Distribution of the four pangene categories on Chr 1 and Chr 2 for (a) A.
- A dashed line visualises the separation of the upper and lower half of the chromosomes.
- For Chr 1 the general picture is similar in all three datasets, i.e., RPKM values are typically above the median value at the upper half (i.e., the region closest to the origin of replication), but lower at the region surrounding the terminus, independent of growth conditions.
- More- over, the detailed map shows that region “ii”, which is densely populated with shell genes, differs from the remaining lower half of Chr 1 by being expressed far below median in V.
- Similar to Chr 1, little difference could be determined between the slow- and the fast- growing datasets of Chr 2..
- The global trend described above can be explained by generally higher expression levels of all pangene categor- ies located close to ori1, or, higher expression of three or less of the four pangene categories.
- To discriminate be- tween the two alternatives, we calculated the RPKM me- dian value for each pangene category, and compared the median values for genes located on the upper or lower halves of Chr 1 (Table 1).
- First, we mapped pangenes to their chromosomal positions and revealed that core and softcore genes are found heavily biased to- wards the ori1 of Chr 1.
- Shell genes are, in contrast, overrepresented at the opposite part of Chr 1 (i.e., close to ter).
- This trend is caused by higher expression of all pangene categories at fast-growing conditions, whereas softcore, shell and cloud genes are responsible for biased (higher) express- ing on the upper half of Chr 1 at slow-growing conditions..
- Pangene categories are non-randomly distributed on Chr 1 In this work we report a clear pattern where core/softcore genes are overrepresented on the upper half of Chr 1 of Vibrionaceae, particularly at regions corresponding to 10–.
- 11 and 1–2 O’clock on Chr 1, and shell/cloud genes are overrepresented in the ter1 region (Fig.
- In comparison, no clear pattern was recorded for Chr 2, i.e., the distribu- tion of pangenes appear generally independent of location..
- Table 1 Comparison of gene expression levels for pangenes located on the upper or lower halves of Chr 1.
- Q 1 is defined as the middle number between the smallest number and the median (i.e., the second quartile Q 2.
- b Adjusted P-values from Wilcoxon signed-rank test, to test if Q 2 values (median) of genes located on the upper half of Chr 1 are significantly different from Q 2.
- values of genes located on the lower half.
- Rocha (2006) showed that genes involved in translation and transcription in four Vibrio species are typically found close to ori1 of Chr 1.
- For ex- ample, genes that encode ribosomal RNA and ribosomal proteins are found clustered in the upper half of Chr 1, and are expressed at extremely high levels, which support this hypothesis..
- natriegens, core, softcore, shell and cloud genes are all expressed at higher levels on the upper half of the chromosome compared to the lower half.
- ori1 and ter1 of Chr 1 are located at the old and new poles, respectively,.
- whereas ori2 and ter2 of Chr 2 stretches from the new pole towards the cell’s center, respectively (Fig.
- The organization of Chr 1 and Chr 2 in V.
- Given a non-random structural organization of the genes (as hypothesized above), this then suggests to us that there is a link between gene placement and their function, and that the underlying reasons for the strong distribution pattern could be very complex.
- In this respect the bipartite DNA organization of Vibrionaceae represents a special case because Chr 1 stretches from pole to pole, whereas Chr 2 prolongates from the new pole towards the cell center, thus suggesting that the chromatin density var- ies between the two halves of the cell.
- 5 Subcellular distribution of Chr 1 and Chr 2 in V.
- Coloured core gene clusters (related to motility, peptidoglycan biosynthesis and ribosomal proteins) represent core gene products that co- localize with growth/survival-related reactions in the old pole of the cell.
- Two replication origins on Chr 1 indicate multifork replication.
- Active growth zones are indicated with blue dashed lines along the axis of the cell.
- The annotation of the 124 genome se- quences resulted in a total of 555,513 annotated protein sequences..
- number of papers published in PubMed) to study the distribution of core, softcore, shell and cloud genes on Chr 1 and Chr 2.
- The 11 species were used to study the exact chromosomal positions of core and shell genes on Chr 1 and Chr 2.
- The DoriC database [57] was used to locate ori1 and ori2 in Chr 1 and Chr 2 to subsequently center the plotted chromosomes at origin of replication, respectively at mioC on Chr 1 and rtcB on Chr 2.
- The quality of the reads was checked using FastQC [58].
- RPKM median to make global expression maps for each of the three datasets..
- Significance of gene distribution on either the upper or lower half of the chromosomes was performed using R’s chisq.test() function for the non-parameteric chi-squared test (see Additional file 4).
- Significance of gene expres- sion between gene classes located on the upper or lower half of the chromosomes was performed using R’s wil- cox.test() function for unpaired Wilcoxon signed-rank tests (see Additional file 4).
- Complete list of the 124 Vibrionaceae genomes used in this study..
- «upper half» and «lower half» of Chr 1 and Chr 2 of 11 representative Vibrionaceae genomes..
- upper half ” and “ lower half ” of Chr 1 and Chr 2..
- TK did statistical analyses and contributed to the writing of the manuscript.
- The funder had no role in study design, data collection and analysis or preparation of the manuscript..
- A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae.
- Synchronous termination of replication of the two chromosomes is an evolutionary selected feature in Vibrionaceae.
- Genomic location of the major ribosomal protein gene locus determines Vibrio cholerae global growth and infectivity.
- Transcriptomic profiling of the oyster pathogen Vibrio splendidus opens a window on the evolutionary dynamics of the small RNA repertoire in the Vibrio genus.
- Functional genomics of the rapidly replicating bacterium Vibrio natriegens by CRISPRi..
- Construction of a fur null mutant and RNA-sequencing provide deeper global understanding of the Aliivibrio salmonicida Fur regulon.
- Transcriptional regulation of the proton-translocating ATPase (atpIBEFHAGDC) operon of Escherichia coli: control by cell growth rate.
- Distinct segregation dynamics of the two Vibrio cholerae chromosomes.
- Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli.
- Nucleolus-like compartmentalization of the transcription machinery in fast-growing bacterial cells.
- Modulation of chemical composition and other parameters of the cell at different exponential growth rates.
- High-resolution mapping of the spatial organization of a bacterial chromosome

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