Viral reproduction and replication

Most contemporary virologists use the term replication to indicate either the production of new virus particles or viral genomes. Because these are very different processes, during the preparation of the fourth edition of the textbook Principles of Virology, the authors decided to use the word reproduction to designate the production of new infectious virus particles, and replication when referring to nucleic acid synthesis. Recently I learned from Bill Summers, speaking at ASV 2019, how the historical use of these two words reflects our evolving concept of virus.

While we have understood for 150 years that viruses cause disease, their physical and biological properties were not always clear. An early definition was that the infectivity of agents causing diseases of plants was ‘filtrable’, leading Beijerinck in 1898 to call them ‘contagious living fluids’. When bacteriophages were first visualized by the electron microscope in 1939, it was obvious that viruses were particulate. The crystallization of tobacco mosaic virus in 1935 lead many to think that viruses were not organisms but chemicals. Stanley, who carried out this work, thought that viruses were infectious proteins!

If viruses were chemicals, then how did they multiply? As Summers writes:

It is interesting to note that the discussion during this period was almost invariably framed in terms of “reproduction,” firmly locating the problem in the realm of biology, not “replication,” a later term favored by the chemists and now part of the modern discourse in virology.

At this time the word ‘replication’ had not entered into lexicon of virologists. Not until 1952, when Hershey and Chase showed that DNA is the genetic material of viruses, did ‘replication’ begin to be used by those studying viruses. In Luria’s 1953 textbook General Virology, the term reproduction can be found many times, but replication only appears twice. The following sentence beautifully illustrates the distinct usage of the two words in 1953 (emphasis mine):

The results suggest a special mode of phage reproduction, in which the chromosomes are replicated by a linear, zipper-like mechanism.

As Summers points out, today nearly every virologist uses the word replication to mean either the synthesis of new virus particles or new genomes. We did the same for the first two editions of Principles of Virology. I’m not sure when replication became ensconced in the virology lexicon, but I feel that having separate terms for production of nucleic acids and virus particles is more precise, removing ambiguity about what is being discussed.

When we first wrote Principles of Virology, we emulated Luria’s General Virology in presenting principles and patterns, not patchworks. Little did we know that we would also return to Luria’s use of reproduction and replication to describe distinct processes.

{ 4 comments… add one }
  • Victor 27 July 2019, 3:45 pm

    I read with keen interest your post about replication vs. reproduction and I had to say that I’m a little disappointed. The use of the term reproduction belongs to microorganisms that actually reproduce (either sexually or asexually). I don’t know what was the thinking behind Luria’s Virology but my guess is that because of a lack of a better term they ”borrowed” the term from the field of bacteriology. Why do I think so, because I’ve seen many Virologists that explore the field of bacterial secondary infection using the term bacteria ”replication”. Which is wrong. Either is bacterial growth or yes you got it right, reproduction . So to see once again how pure virologists for a lack of a better term and maybe a lack of deeper understanding of other fields in microbiology, they decided to use not the best terminology (this is just a personal opinion) it is disappointing. Yes it may be ok to use the term “reproduction” in the Virology field but it will create confusion, especially with students that are also studying bacteriology, micology and parasitology.
    Once again, this is my opinion and it doesn’t change at all the great respect and admiration I have for yOut or the editors of the Principles.

    Cheers,

    V

  • Angel L. 28 July 2019, 9:38 am

    Wow, I was so excited to hear there’s people discussing about this topic. When I was teaching Virology at the University of Havana between 2005 and 2009 I was already making this distinction after I noticed a huge confussion among students. I absolutely agree with the need to separate both terms, but I also think that ‘reproduction’ might not be adequate. I was using ‘multiplication’ instead (actually, the equivalent Spanish word ‘multiplicación’), to distinguish it from the reproduction event of living organisms. However I’m not totally sure that the literal translation ‘multiplication’ is the best choice. Cheers.

  • Bill Summers 14 August 2019, 9:45 am

    Just a comment to add some more historical context: Thinking back to the first half of the 20th century, there was more mystery connected with the question of “how like begets like” in the large sense. Why to dogs give birth to dogs and not, say, cats? Embryology (not “evo-devo”) was hot science: how do precise forms come about? Microbes were quite marginal to mainstream biology, and there was debate as to whether they even had “genes.” There was even a tendency to consider the entire culture as the “organism” rather than the individual cell. We still speak of the various “phases” of growth of the culture as a whole (lag phase, log phase, stationary phase, etc.). Luria was educated as a physician, initially in histology, and certainly had a biological feel for his science. “Reproduction” was what concerned biologists because they were looking at frogs, sea urchins, fruit flies, rabbits, and human beings (and sometimes, plants). A great contribution of the early molecular biologists, I think, was to establish the link between reproduction of the whole, with replication of the parts. The simplicity (and beauty) of this connection apparently was disappointing to Max Delbruck, who once told me that if he had known in advance that the problem of “like begets like” would devolve to the stereochemistry of base pairs, he might never have taken it up.

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