Essential gene acquisition destabilizes plasmid inheritance.

Tanita Wein,Fenna T Stücker,Tal Dagan,Katrin Hammerschmidt,Yiqing Wang,Myriam Barz,R Craig Maclean

doi:10.1371/journal.pgen.1009656

Abstract

Extra-chromosomal genetic elements are important drivers of evolutionary transformations and ecological adaptations in prokaryotes with their evolutionary success often depending on their ‘utility’ to the host. Examples are plasmids encoding antibiotic resistance genes, which are known to proliferate in the presence of antibiotics. Plasmids carrying an essential host function are recognized as permanent residents in their host. Essential plasmids have been reported in several taxa where they often encode essential metabolic functions; nonetheless, their evolution remains poorly understood. Here we show that essential genes are rarely encoded on plasmids; evolving essential plasmids in Escherichia coli we further find that acquisition of an essential chromosomal gene by a plasmid can lead to plasmid extinction. A comparative genomics analysis of Escherichia isolates reveals few plasmid-encoded essential genes, yet these are often integrated into plasmid-related functions; an example is the GroEL/GroES chaperonin. Experimental evolution of a chaperonin-encoding plasmid shows that the acquisition of an essential gene reduces plasmid fitness regardless of the stability of plasmid inheritance. Our results suggest that essential plasmid emergence leads to a dose effect caused by gene redundancy. The detrimental effect of essential gene acquisition on plasmid inheritance constitutes a barrier for plasmid-mediated lateral gene transfer and supplies a mechanistic understanding for the rarity of essential genes in extra-chromosomal genetic elements.

Highlights

Plasmids are autonomously replicating genetic elements that are prominent in prokaryotes and have been studied extensively due to their contribution to lateral gene transfer
Prokaryotic plasmids have been the focus of investigation in the context of bacterial survival under growth limiting conditions with the prime example of resistance to antibiotics and heavy metals
We investigate the evolution of plasmids that encode for genes previously identified as essential for bacterial life

Summary

Introduction

Plasmids are autonomously replicating genetic elements that are prominent in prokaryotes and have been studied extensively due to their contribution to lateral gene transfer. E.g., those that supply resistance against antibiotics (e.g., [1,2]) or heavy metals (e.g., [3,4]) enable their host to survive under transient selective conditions. Environmental conditions are rarely constant; a decrease in the strength of selection for plasmidencoded beneficial genes–e.g., due to fluctuating abundance of growth limiting factors–may lead to plasmid loss and extinction. Plasmids that supply the host with essential functions, i.e., whose benefit to the host is less dependent on temporary environmental conditions, may persist over longer time scales and become an integral component of the lineage genome in the form of chromids [10]. The evolution of plasmids encoding essential genes may depend on the evolution of stable plasmid-host interactions

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Conclusion