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The pan-genome as a shared genomic resource: mutual cheating, cooperation and the black queen hypothesis

Matthew S. Fullmer,Shannon M. Soucy,J. Gogarten

Published 2015 in Frontiers in Microbiology

ABSTRACT

Cells have long been recognized as life’s building blocks (e.g., Virchow’s dictum “omnis cellula e cellula,” Virchow, 1860). Specifically, a cell’s genome is considered the repository of genetic information that pairs with the cellular machinery to determine the organism’s phenotype. Except for rare circumstances, themajority of a genome is passed on from ancestor to descendant, although the acquisition of genes from organisms that are not direct ancestors is recognized to play an important role in evolution (Swithers et al., 2012). Jeffrey Lawrence, in discussing minimal genome size proposed a meta-cell model (Lawrence, 1999), in which many micelles (small vesicles containing resources, products, and genes) exchange genes frequently. Genes temporarily reside in a micelle and direct the synthesis of compounds important for replication. A micelle only can replicate when all compounds necessary for division have been generated. However, at each point in time only a fraction of the necessary genes are present in an individual micelle. This model relies on gene transfer being so frequent that each of the genes that encode necessary functions visits the individual micelles often enough to allow for sufficient synthesis of the necessary gene products for future micelle divisions. The meta-cell can be considered an organism, whose genome is divided into a network of micelles. Lawrence’s metacell model is reminiscent of Woese’s progenote (Woese, 1998) and Kandler’s pre-cell populations (Kandler, 1994) that were postulated to have existed early in evolution before genes coalesced into genomes.

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