Indirect Fitness Benefits Enable the Spread of Host Genes Promoting Costly Transfer of Beneficial Plasmids.
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.
Institut National de la Santé et de la Recherche Médicale, U1001, Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
Tatiana
T
Dimitriu
Institut National de la Santé et de la Recherche Médicale, U1001, Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
Dusan
D
Misevic
Institut National de la Santé et de la Recherche Médicale, U1001, Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
Chantal
C
Lotton
Georgia Institute of Technology, School of Biology, Atlanta, Georgia, United States of America.
Sam P
SP
Brown
Institut National de la Santé et de la Recherche Médicale, U1001, Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
Ariel B
AB
Lindner
Institut National de la Santé et de la Recherche Médicale, U1001, Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
François
F
Taddei
D000465:Algorithms; D001419:Bacteria / Q000235:genetics*; D003227:Conjugation, Genetic; D024881:Drug Resistance, Bacterial / Q000235:genetics*; D004926:Escherichia coli / Q000235:genetics; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D005798:Genes, Bacterial / Q000235:genetics*; D056084:Genetic Fitness; D005828:Genetics, Population; D020071:Interspersed Repetitive Sequences / Q000235:genetics; D008957:Models, Genetic; D010957:Plasmids / Q000235:genetics; D012641:Selection, Genetic