Compensatory mutations reducing the fitness cost of plasmid carriage occur in plant rhizosphere communities

Abstract

Plasmids drive bacterial evolutionary innovation by transferring ecologically important functions between lineages, but acquiring a plasmid often comes at a fitness cost to the host cell. Compensatory mutations, which ameliorate the cost of plasmid carriage, promote plasmid maintenance in simplified laboratory media across diverse plasmid-host associations. Whether such compensatory evolution can occur in more complex communities inhabiting natural environmental niches where evolutionary paths may be more constrained is, however, unclear. Here we show a substantial fitness cost of carrying the large conjugative plasmid pQBR103 in Pseudomonas fluorescens in the plant rhizosphere. This plasmid fitness cost could be ameliorated by compensatory mutations affecting the chromosomal global regulatory system gacA/gacS, which arose rapidly in plant rhizosphere communities and were exclusive to plasmid carriers. These findings expand our understanding of the importance of compensatory evolution in plasmid dynamics beyond simplified lab media. Compensatory mutations contribute to plasmid survival in bacterial populations living within complex microbial communities in their natural environmental niche.

Microbial evolution through horizontal gene transfer by mobile genetic elements

“…Mutations in TrfA44 can inhibit its interaction with DnaB, resulting in mitigation of the fitness cost (Yano et al, 2016). Several studies have shown that compensatory mutations can ameliorate the cost of carriage of the plasmid pQBR103 in Pseudomonas spp., not only under laboratory conditions (Harrison et al, 2015(Harrison et al, , 2016, but also in the rhizosphere (Bird et al, 2023). Mutations in the GacA/GacS system encoded on the host chromosome can reduce the fitness cost of plasmid carriage (Harrison et al, 2015).…”