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Flexibility and symmetry of prokaryotic genome rearrangement reveal lineage-associated core-gene-defined genome organizational frameworks.

ABSTRACT:

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The prokaryotic pangenome partitions genes into core and dispensable genes. The order of core genes, albeit assumed to be stable under selection in general, is frequently interrupted by horizontal gene transfer and rearrangement, but how a core-gene-defined genome maintains its stability or flexibility remains to be investigated. Based on data from 30 species, including 425 genomes from six phyla, we grouped core genes into syntenic blocks in the context of a pangenome according to their stability across multiple isolates. A subset of the core genes, often species specific and lineage associated, formed a core-gene-defined genome organizational framework (cGOF). Such cGOFs are either single segmental (one-third of the species analyzed) or multisegmental (the rest). Multisegment cGOFs were further classified into symmetric or asymmetric according to segment orientations toward the origin-terminus axis. The cGOFs in Gram-positive species are exclusively symmetric and often reversible in orientation, as opposed to those of the Gram-negative bacteria, which are all asymmetric and irreversible. Meanwhile, all species showing strong strand-biased gene distribution contain symmetric cGOFs and often specific DnaE (α subunit of DNA polymerase III) isoforms. Furthermore, functional evaluations revealed that cGOF genes are hub associated with regard to cellular activities, and the stability of cGOF provides efficient indexes for scaffold orientation as demonstrated by assembling virtual and empirical genome drafts. cGOFs show species specificity, and the symmetry of multisegmental cGOFs is conserved among taxa and constrained by DNA polymerase-centric strand-biased gene distribution. The definition of species-specific cGOFs provides powerful guidance for genome assembly and other structure-based analysis.

Importance

Prokaryotic genomes are frequently interrupted by horizontal gene transfer (HGT) and rearrangement. To know whether there is a set of genes not only conserved in position among isolates but also functionally essential for a given species and to further evaluate the stability or flexibility of such genome structures across lineages are of importance. Based on a large number of multi-isolate pangenomic data, our analysis reveals that a subset of core genes is organized into a core-gene-defined genome organizational framework, or cGOF. Furthermore, the lineage-associated cGOFs among Gram-positive and Gram-negative bacteria behave differently: the former, composed of 2 to 4 segments, have their fragments symmetrically rearranged around the origin-terminus axis, whereas the latter show more complex segmentation and are partitioned asymmetrically into chromosomal structures. The definition of cGOFs provides new insights into prokaryotic genome organization and efficient guidance for genome assembly and analysis.

SUBMITTER: Kang Y

PROVIDER: S-EPMC4251990 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The increasing resistance of Plasmodium, the malaria parasites, to multiple commonly used drugs has underscored the urgent need to develop effective antimalarial drugs and vaccines. The new direction of genomics-driven target discovery has become possible with the completion of parasite genome sequencing, which can lead us to a better understanding of how the parasites develop the genetic variability that is associated with their response to environmental challenges and other adaptive phenotypes.We present the results of a comprehensive analysis of the genomes of six Plasmodium species, including two species that infect humans, one that infects monkeys, and three that infect rodents. The core genome shared by all six species is composed of 3,351 genes, which make up about 22%-65% of the genome repertoire. These components play important roles in fundamental functions as well as in parasite-specific activities. We further investigated the distribution and features of genes that have been expanded in specific Plasmodium lineage(s). Abundant duplicate genes are present in the six species, with 5%-9% of the whole genomes composed lineage specific radiations. The majority of these gene families are hypothetical proteins with unknown functions; a few may have predicted roles such as antigenic variation.The core genome components in the malaria parasites have functions ranging from fundamental biological processes to roles in the complex networks that sustain the parasite-specific lifestyles appropriate to different hosts. They represent the minimum requirement to maintain a successful life cycle that spans vertebrate hosts and mosquito vectors. Lineage specific expansions (LSEs) have given rise to abundant gene families in Plasmodium. Although the functions of most families remain unknown, these LSEs could reveal components in parasite networks that, by their enhanced genetic variability, can contribute to pathogenesis, virulence, responses to environmental challenges, or interesting phenotypes.

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Flexibility and symmetry of prokaryotic genome rearrangement reveal lineage-associated core-gene-defined genome organizational frameworks.

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