Abstract

A pangenome is the complete set of genes (core and accessory) present in a phylogenetic clade. We hypothesize that a pangenome’s accessory gene content is structured and maintained by selection. To test this hypothesis, we interrogated the genomes of 40 Pseudomonas species for statistically significant coincident (i.e., co-occurring/avoiding) gene patterns. We found that 86.7% of common accessory genes are involved in 1 coincident relationship. Further, genes that co-occur and/or avoid each other—but are not vertically inherited—are more likely to share functional categories, are more likely to be simultaneously transcribed, and are more likely to produce interacting proteins, than would be expected by chance. These results are not due to coincident genes being adjacent to one another on the chromosome. Together, these findings suggest that the accessory genome is structured into sets of genes that function together within a given strain. Given the similarity of the Pseudomonas pangenome with open pangenomes of other prokaryotic species, we speculate that these results are generalizable.

Highlights

  • The mechanisms governing the existence of the pangenome—the totality of genes across a given set of genomes (Tettelin et al 2005)—have been debated, with evidence being presented for both neutral and selective processes (McInerney et al 2017a, 2017b; Shapiro 2017)

  • Some evidence suggests that the accessory gene content within pangenomes has arisen as a consequence of extensive horizontal gene transfer (HGT) coupled with large effective population size and evolve neutrally (Andreani et al 2017)

  • Others argue that accessory genome evolution is dominated by selective pressures, and that diversity is maintained by selection acting on gene gain by horizontal acquisition, as well as gene loss (McInerney et al 2017b; Bobay and Ochman 2018; Goyal 2018)

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Summary

Introduction

The mechanisms governing the existence of the pangenome—the totality of genes across a given set of genomes (Tettelin et al 2005)—have been debated, with evidence being presented for both neutral and selective processes (McInerney et al 2017a, 2017b; Shapiro 2017). It would be reasonable to expect, at least in some cases, that genes whose interaction would be detrimental to the host to avoid being in the same genome. In this way, we expect that genes, which consistently co-occur or avoid each other across a large pangenome to be under selective pressures to maintain these patterns. We use gene pair information to ask whether a portion of the accessory gene content is governed by selective pressure

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