Abstract
Bacterial genomes typically consist of one large chromosome, but can also include secondary replicons. These so-called multipartite genomes are scattered on the bacterial tree of life with the majority of cases belonging to Proteobacteria. Within the class gamma-proteobacteria, multipartite genomes are restricted to the two families Vibrionaceae and Pseudoalteromonadaceae. Whereas the genome of vibrios is well studied, information on the Pseudoalteromonadaceae genome is much scarcer. We have studied Pseudoalteromonadaceae with respect to the origin of the chromid, how pangene categories are distributed, how genes are expressed relative to their genomic location, and identified chromid hallmark genes. We calculated the Pseudoalteromonadaceae pangenome based on 25 complete genomes and found that core/softcore are significantly overrepresented in late replicating sectors of the chromid, regardless of how the chromid is replicated. On the chromosome, core/softcore and shell/cloud genes are only weakly overrepresented at the chromosomal replication origin and termination sequences, respectively. Gene expression is trending downwards with increasing distance from the chromosomal oriC, whereas the chromidal expression pattern is more complex. Moreover, we identified 78 chromid hallmark genes, and BLASTp searches suggest that the majority of them were acquired from the ancestral gene pool of Alteromonadales. Finally, our data strongly suggest that the chromid originates from a plasmid that was acquired in a relatively recent event. In summary, this study extends our knowledge on multipartite genomes, and helps us understand how and why secondary replicons are acquired, why they are maintained, and how they are shaped by evolution.
Highlights
Multipartite genomes are recognized by the concurrent presence of multiple replicons, i.e., cells contain one or more large replicons in addition to the chromosome (Harrison et al 2010)
We have studied Pseudoalteromonadaceae with respect to the origin of the chromid, how pangene categories are distributed, how genes are expressed relative to their genomic location, and identified chromid hallmark genes
We identified 78 chromid hallmark genes, and BLASTp searches suggest that the majority of them were acquired from the ancestral gene pool of Alteromonadales
Summary
Multipartite genomes are recognized by the concurrent presence of multiple replicons, i.e., cells contain one or more large replicons in addition to the chromosome (Harrison et al 2010). The majority of bacteria with multipartite genomes are associated with high tolerance to abiotic stresses, or are associated with animals, human, or plants as pathogens or symbionts (Misra et al 2018). This observation, in addition to other data, has prompted scientists to hypothesize that multipartite genomes play crucial roles in the successful spread and establishment of bacteria into a broad range of ecological niches (Heidelberg et al 2000). It has been suggested that the presence of multiple replicons allows bacteria to contain larger genomes, and may reduce the time required to complete replication allowing for rapid cell growth and division (diCenzo et al 2014). We recently proposed a hypothesis that the presence of two large replicons allows for intracellular spatial separation of different categories of genes, and that there is a link
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