Bacterial Sex Explained: the French Connection

“I give lectures on the history of bacterial genetics, and I always said that the Americans had the wherewithal to discover sex in bacteria, but it took the Frenchmen to work out all the fine details.”                                  

Stanley Falkow

 

Plants and animals, you and I, inherit our genes from parents. If we reproduce, we pass our genes to our offspring. Inheritance is vertical, from parent to child to grandchild.

Now “imagine a different world where friends and colleagues can swap genes at will,” wrote Ed Yong, in his book about the microbial world, I Contain Multitudes: The Microbes Within Us and a Grandeur View of Life. If your child is lactose intolerant, you can get him the gene that enables him to comfortably digest the mozzarella on his pizza. Or you can borrow the genes that can make your wife resistant to breast cancer. This is the strange world that bacteria live in. Bacteria reproduce by fission: splitting in half to produce identical daughter cells. Their kind of sex is horizontal and separate from reproduction. Bacterial easily and promiscuously exchange genes among neighbors and even different bacterial species.

Joshua Lederberg and Edward Tatum discovered that bacteria could recombine genes in 1946. But it took another decade of research before the exotic details of bacterial sex were clarified. Lederberg incorrectly assumed that two bacterial cells mutually exchanged genes, merging their entire genomes, analogous to sexual reproduction in animals and plants.

He called the process “conjugation”, referring to the sexual conjugation that sometimes occurs between two different mating-types of Paramecium, the single-celled protists in pond scum.

Over the next decade, results from laboratories in London, Milan, and ultimately Paris revealed the exotic details of bacterial sex. In 1952, the Irish physician William Hayes reported that the gene transferr occurred in one direction—from male to female. Furthermore, only part of the bacterial genome was transferred.

 

WHayes (Royaumont)

William Hayes presenting evidence for uni-directional gene transfer in bacteria at the Second International Symposium on Microbial Genetics in Pallanza, Italy, September 1952.

 

These striking differences from the vertical inheritance of animals and plants were not completely understood until 1955, when researchers at the Pasteur Institute performed the “coitus interruptus” experiment. After mixing together the male and female bacteria, and then allowing the mating to proceed, the researchers interrupted the gene transfer by vigorously swirling the mating pairs with a Waring blender. At different time intervals, the researchers sheared apart the mating pair, and then analyzed which genetic markers get trasferred first, next and later. They realized that the linear strand of male DNA was gradually, sequentially transferred into the female cell. They called this the “spaghetti hypothesis,” imagining that the female bacterium slurped up the male strand of DNA, like one might suck up a long pasta noodle. With most matings, only a portion of the male DNA strand gets transferred, like when the pasta noodle breaks before the entire noodle gets sucked up.

 

 

 

Box1 057 BWright EWollman EML 50

B. Wright, Elie Wollman, and Esther Lederberg, 1950.

 

The French researchers, Elie Wollman and Francoise Jacob, were completely astounded by the results of the coitus interruptus experiment. Wollman told Horace Judson, recorded in The Eighth Day of Creation, “the fact itself could not be anticipated. I mean, nobody had ever thought before of a chromosome which would be transferred from one end . . . this was–this was unforeseeable!”

It would be decades before the scientific community fully realized the implications promiscuous bacterial sex. One deadly result is the emergence of super-bugs, pathogens resistant to multiple antibiotics. The process driving the emergence of super-bugs is bacterial sex.

 

 

Stanley Falkow. 14 May 2015. Author’s interview at the Department of Microbiology and Immunology, Stanford University.

Yong, E. 2016. I Contain Multitudes: The Microbes Within Us and a Grander View of Life. Harper Collins, Kindle Edition.

http://www.pnas.org/content/23/7/378.short

Sonneborn, T. M. 1937. “Sex, Sex Inheritance and Sex Determination in Paramecium Aurelia.” Proceedings of the National Academy of Sciences. 23, 378-385.

Lederberg, J., Cavalli, L. I., and Lederberg, E. M. 1952. “Sex Compatibility in Escherichia coli.” Genetics 37, 720-730.

Hayes, W. 1952. “Recombination in Bacterium coli K-12: Uni-directional Transfer of Genetic Material.” Nature 169, 118-119.

Jacob F, Wollman E. 1961. Sexuality and the Genetics of Bacteria. Academic Press, New York.

Judson, H. F. 1996. The Eighth Day of Creation: Makers of the Revolution in Biology Cold Spring Harbor Laboratory Press. Commemorative Edition.

Schindler, T. 2018. “Bacterial Sex: the Promiscuos Process Driving Antibiotic Resistance.”   https://www.statnews.com/2018/02/20/antibiotic-resistance-bacterial-sex/