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

Abstract

<i>Background</i> - The genome of <i>Vibrionaceae</i> 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 (<i>ori1</i>). This is believed to be a growth optimization strategy to satisfy the high demand of essential growth factors during fast growth. The relationship between <i>ori1</i>-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 <i>ori1</i> and if expression of all <i>ori1</i>-proximate genes is increased during fast growth, or if expression is selectively elevated for certain gene categories.<p><p>

<i>Results</i> - We calculated the pangenome of all complete genomes from the <i>Vibrionaceae</i> 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 <i>ori1</i>, while shell genes were overrepresented at the opposite part of Chr 1 (i.e., close to <i>ter1</i>). RNA-seq of <i>Aliivibrio salmonicida</i> and <i>Vibrio natriegens</i> showed global gene expression patterns that consistently correlated with chromosomal distance to <i>ori1</i>. 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.<p><p>

<i>Conclusion</i> - The pangene categories were non-randomly organized on Chr 1, with an overrepresentation of core and softcore genes around <i>ori1</i>, and overrepresentation of shell and cloud genes around <i>ter1</i>. Furthermore, we mapped our gene distribution data on to the intracellular positioning of chromatin described for <i>V. cholerae</i>, 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.