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Work by a husband-and-wife team of virologists is shedding new light on an old scientific dispute: did viruses emerge before or after the development of cellular life? Until recently, many scientists believed that viruses only appeared after the first cells emerged on the primordial Earth. However, the recent discovery of strange genes in giant viruses is leading some scientists to suggest that the ancestors of viruses evolved before cells.
Are they alive or aren’t they?
Giant viruses, which were first described in 2003, straddle the gap between viruses and bacteria. Despite the fact that viruses undergo natural selection and reproduce by creating multiple copies of themselves through self-assembly – an ability which University of Cape Town virologist Ed Rybicki considers sufficient to qualify them as living things – it has long been argued that viruses are not truly alive, since they lack the machinery required to replicate their genes: instead, they have to make use of the genes belonging to the cells they infect. Consequently, most scientists have argued that viruses could only have emerged after the appearance of the first cells on Earth. Nobel Laureate and Harvard biochemist Jack Szostak espouses this view of viruses, in an interview with science journalist Carrie Arnold in Quanta magazine: “They rely on cellular machinery to help with their replication, so they need to have some sort of primitive cell to make use of that machinery” (Hints of Life’s Start Found in a Giant Virus, July 10, 2014). However, giant viruses possess some genes which are involved in replication, which suggests that they may have once been free-living organisms that devolved into viruses.
In 2013, husband-and-wife team Chantal Abergel and Jean-Michel Claverie discovered the pithovirus, a remarkable virus with some 500 genes – some viruses have as few as four – which are used for complex tasks, such as making proteins and repairing and replicating DNA. Because they possess some of their own replication machinery, pithoviruses are quite different from most viruses, which copy themselves by hijacking their host’s molecular machinery.
As far back as 2003, Abergel and Claverie helped identify the mimivirus (illustrated above, courtesy of Wikipedia and InvaderXan), which was originally thought to be a parasitic bacterium, on account of its large size (>0.7 micrometers) and genomic complexity (>1000 genes). When the husband-and-wife team looked at the organism through a microscope, they instantly recognized the distinctive shape of a virus. More recently, they discovered an even bigger virus growing in amoebae, which they christened the pandoravirus on account of its surprising lack of similarity with previously described viruses. Abergel and Claverie reported on their discovery last year, in Science magazine (Vol. 341 no. 6143, 19 July 2013, pp. 281-286, DOI: 10.1126/science.1239181). As Abergel put it: “More than 90 percent of its genes did not resemble anything else found on Earth.” And how many genes did it have? A staggering 2,500 (by comparison, the bacterium E. coli has 4,300).
A fourth domain of life?
Some researchers contend that the genetic uniqueness of giant viruses indicates that they merit their own branch on the tree of life, as a fourth domain alongside bacteria, archaea and eukaryotes (organisms such as plants, animals, fungi and protists, whose cells contain a nucleus). And it would be a very old branch, too. In a 2012 study in the journal BMC Evolutionary Biology (12:156, doi:10.1186/1471-2148-12-156), Gustavo Caetano-Anolles, a bioinformatics specialist at the University of Illinois, Urbana-Champaign, traced the evolutionary history of proteins occurring in several giant viruses and concluded that these viruses “represent a form of life that either predated or coexisted with the last universal common ancestor,” an organism which is estimated to have lived some 3.5 to 3.8 billion years ago.
Koonin’s Virus World theory
Evolutionary biologist Eugene Koonin has even suggested that modern cells evolved from viruses. In her report for Quanta magazine (July 10, 2014), science journalist Carrie Arnold handily summarizes Koonin’s proposal:
According to his theory, dubbed the Virus World, the ancestors of modern viruses emerged when all life was still a floating stew of genetic information, amino acids and lipids. The earliest pieces of genetic material were likely short pieces of RNA with relatively few genes that often parasitized other floating bits of genetic material to make copies of themselves. These naked pieces of genetic information swapped genes at a primeval genetic flea market, appropriating hand-me-downs from other elements and discarding genes that were no longer needed.
Over time, Koonin argues, the parasitic genetic elements remained unable to replicate on their own and evolved into modern-day viruses that mooch off their cellular hosts. The genes they parasitized began to evolve different types of genetic information and other barriers to protect themselves from the genetic freeloaders, which ultimately evolved into cells.
A curious omission: Koonin himself believes the emergence of life on Earth was overwhelmingly unlikely
What I find most astonishing about this report, however, is that it makes no mention of Koonin’s valuable work in demonstrating that the origin of life was an astronomically improbable event. Indeed, Koonin estimates that the likelihood of life’s evolving anywhere in the observable universe over its 13.8-billion-year lifetime is just 1 in 101,018 – that’s 1 in 1 followed by 1,018 zeroes! And that’s an estimate that Koonin himself describes as generous, in an article he wrote in 2007, titled, The Cosmological Model of Eternal Inflation and the Transition from Chance to Biological Evolution in the History of Life (Biology Direct 2 (2007): 15, doi:10.1186/1745-6150-2-15). In the passage below, the term “O-region” refers to an observable universe, like our own. Koonin considers the emergence of life in our observable universe to be such an unlikely event that he is forced to postulate the existence of a vast and possibly infinite number of universes like our own, in order to make the origin of life somewhere reasonably probable. Even assuming the existence of self-replicating RNA molecules, the difficulty of generating a translation-replication system (which is found in all cellular organisms) by a process of Darwinian selection is truly staggering. As Koonin puts it:
In other words, even in this toy model that assumes a deliberately inflated rate of RNA production, the probability that a coupled translation-replication emerges by chance in a single O-region is P < 10-1018. Obviously, this version of the breakthrough stage can be considered only in the context of a universe with an infinite (or, at the very least, extremely vast) number of O-regions.
The argument presented in Koonin’s peer-reviewed paper has been republished in his recent book, The Logic of Chance: The Nature and Origin of Biological Evolution (Upper Saddle River: FT Press, 2011, ISBN 978-0-13-262317-9), which can be viewed online.
A new chicken-and-egg paradox relating to the origin of life
Valerian Dolja, a virologist at Oregon State University and a professional colleague of Koonin’s, is a strong supporter of his Virus World theory. She argues that if viruses developed from cells, they should be genetically less diverse than cells, as cells would contain the entire range of genes found in viruses – but in fact, scientists have found that the reverse is the case. Patrick Forterre, a virologist at Paris-Sud University, is another advocate of Koonin’s theory. He points out that viruses are also more diverse than cellular organisms in their methods of reproduction: the latter have only two main methods of reproduction, while viruses have many different methods. Forterre believes, however, that viruses evolved after primitive cells, but before modern cells.
Harvard biochemist Jack Szostak offers a more cautious interpretation of the evidence: although he is willing to accept that parasitic genetic elements (bits of genetic material that use other bits in order to make copies of themselves) may have existed on Earth before cells, he nonetheless insists that true viruses only emerged after cellular organisms did. In her report for Quanta magazine, Carrie Arnold highlights the disagreement between the two camps:
“Whenever you mix a bunch of small RNA molecules together, you get a bunch of parasitic sequences that aren’t good at anything except making copies of themselves faster than anything else,” Szostak said. For these sequences to become similar to modern viruses, they need to parasitize a living cell, not just another strand of RNA.
Dolja disagrees, saying that cells could not have evolved without viruses. “In order to move from RNA to DNA, you need an enzyme called reverse transcriptase,” Dolja said. “It’s only found in viruses like HIV, not in cells. So how could cells begin to use DNA without the help of a virus?”
For their part, Abergel and Claverie propose that giant viruses evolved from a line of cells that lost its ability to replicate on their own and was forced to rely on other cells to copy its DNA. The husband-and-wife team reject the view that life developed from a single common ancestor, arguing instead that competition between several different kinds of cell-like organisms accounts for the diversity of life on Earth today.
What I find most remarkable about the contemporary debate regarding the role of viruses in the origin of life on Earth is that a new chicken-and-egg paradox has received so little attention in the popular science media. On the one hand, Szostak argues convincingly that in order for parasitic genetic elements to become like modern viruses, they need to parasitize a living cell. On the other hand, Dolja contends that cells could not have evolved without viruses, as they need reverse transcriptase (which is found only in viruses) in order to move from RNA to DNA.
In other words, instead of helping to solve the problem of the origin of life on Earth, recent research has only served to highlight one of its central paradoxes. And yet the science media reports the latest discoveries as if the solution is just around the corner. Don’t you find that just a little strange?
What do readers think? Comments are welcome.