Abstract
Bacterial genes that confer crucial phenotypes, such as antibiotic resistance, can spread horizontally by residing on mobile genetic elements (MGEs). Although many mobile genes provide strong benefits to their hosts, the fitness consequences of the process of transfer itself are less clear. In previous studies, transfer has been interpreted as a parasitic trait of the MGEs because of its costs to the host but also as a trait benefiting host populations through the sharing of a common gene pool. Here, we show that costly donation is an altruistic act when it spreads beneficial MGEs favoured when it increases the inclusive fitness of donor ability alleles. We show mathematically that donor ability can be selected when relatedness at the locus modulating transfer is sufficiently high between donor and recipients, ensuring high frequency of transfer between cells sharing donor alleles. We further experimentally demonstrate that either population structure or discrimination in transfer can increase relatedness to a level selecting for chromosomal transfer alleles. Both mechanisms are likely to occur in natural environments. The simple process of strong dilution can create sufficient population structure to select for donor ability. Another mechanism observed in natural isolates, discrimination in transfer, can emerge through coselection of transfer and discrimination alleles. Our work shows that horizontal gene transfer in bacteria can be promoted by bacterial hosts themselves and not only by MGEs. In the longer term, the success of cells bearing beneficial MGEs combined with biased transfer leads to an association between high donor ability, discrimination, and mobile beneficial genes. However, in conditions that do not select for altruism, host bacteria promoting transfer are outcompeted by hosts with lower transfer rate, an aspect that could be relevant in the fight against the spread of antibiotic resistance.
Highlights
mobile genetic element (MGE) such as plasmids or phages are defined by their ability to undergo horizontal gene transfer (HGT) between bacterial hosts [1], and are widespread in nature
Genes can move between cells, sometimes with the donor host cell actively involved in the gene transfer mechanisms
This movement of genes is called horizontal gene transfer, and it increases the prevalence of mobile genes in bacterial populations
Summary
MGEs such as plasmids or phages are defined by their ability to undergo horizontal gene transfer (HGT) between bacterial hosts [1], and are widespread in nature. The population dynamics and evolution of transfer have mostly been studied by focusing on MGEs themselves [7]; transfer is influenced by MGE genes, and by genes of the bacterial host chromosome Both donor [8] and recipient cells [9,10] can regulate transfer, with different donor and recipient genetic backgrounds resulting in as much as eight orders of magnitude variance in the transfer rates for the same plasmid [11,12]. To fully understand the evolution of horizontal gene spread and the natural variation in transfer rates among hosts, we must consider the selective pressures acting on hosts
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