Are there viruses of arsenic-utilizing bacteria?

Mono LakeA salt-loving (halophilic) bacterium which can grow in medium containing arsenic instead of phosphorus has been selected from the microbial community of Mono Lake in California. Arsenic (As) is a chemical analog of phosphorus and is usually toxic because it can enter metabolic pathways in the place of phosphorus. It appears to be incorporated into macromolecules of the bacterium (called GFAJ-1) that normally contain phosphorus, such as nucleic acids and proteins. The identification of bacteria that can utilize arsenic has many metabolic and evolutionary implications. I’m wondering whether there are viruses that infect bacteria such as GFAJ-1.

It has been suggested that Mono Lake contains organisms that are biologically distinct from all others so far discovered on Earth. In other words, organisms like GFAJ-1 that utilize arsenic might represent not just a different branch on the evolutionary tree, but an entire tree altogether. As Henry Bortman writes, “It would strongly suggest that life got started on our planet not once, but at least twice, that the origin of life on Earth was not a freak accident requiring highly specialized circumstances, but a relatively commonplace event.”

These  conclusions seem unlikely. GFAJ-1 is a variant of existing bacteria from the family Halomonadaceae that has been selected to grow in the presence of arsenic. As Ed Yong has written, GFAJ-1 does not depend on arsenic, and there is no evidence that it belongs to a second tree of life on Earth. But let’s step back for a moment and assume that there are organisms on Earth from a second tree of life. Are there viruses that infect them?

Viruses are believed to have existed either before cellular life emerged, or evolved very shortly thereafter. Was the emergence of viruses a freak accident, or are viruses found whenever life evolves? This has been a difficult question to answer since we have evidence on Earth that life evolved just once. Finding viruses that infect members of a second branch of life would suggest – but not prove – that viruses are important for the evolution of life. If no such viruses were found – and we’d have to search very hard to make that conclusion – then it would suggest that they are not needed for life.

Let’s come back to earth and return to GFAJ-1. As far as I know there are no known viruses of this particular type of bacterium (although there are bacteriophages that infect members of the genus Halomonas). Are there viruses of GFAJ-1? If so, can they replicate in GFAJ-1 when the bacteria are propagated in medium containing arsenic in place of phosphorus? Or is the viral replication machinery only able to replicate nucleic acids containing phosphorus? Since GFAJ-1 was selected from the Mono Lake microbial community, it is a reasonable assumption that similar bacteria are present in the lake sediments (although their prevalence there is unknown). In that environment there will always be phosphorus present, so it’s not clear if viruses could have evolved that function when arsenic is substituted for phosphorus.

The research group that identified GFAJ-1 has plenty of work to do to understand the biology and ecology of this bacterium. But there are many interesting viral questions as well, and if I were part of that group, I’d be searching the genome of GFAJ-1 for virus-like sequences, and looking for viruses in the sediments of Mono Lake.

Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Pett-Ridge J, Stolz JF, Webb SM, Weber PK, Davies PC, Anbar AD, & Oremland RS (2010). A Bacterium That Can Grow by Using Arsenic Instead of Phosphorus. Science (New York, N.Y.) PMID: 21127214

Update: The Science article is receiving a great deal of criticism. Rosie Redfield has a very comprehensive review, concluding that “Basically, it doesn’t present ANY convincing evidence that arsenic has been incorporated into DNA (or any other biological molecule).

A new type of enveloped virus?

All known virus particles can be placed into one of two general categories: enveloped or non-enveloped. Viruses that fall into the former category are characterized by a lipid membrane derived from the host cell, and one or more nuclecapsid proteins that interact with the viral genome. A virus that infects an archaeal host may constitute a new category of enveloped viruses. It comprises a membrane vesicle that encloses a circular ssDNA genome which is devoid of nucleic acid-binding nucleoproteins.

Examples of enveloped virions that contain nucleoproteins are shown in the figure below. These include influenza virus (left), a simple retrovirus (center), and a togavirus (right).

The influenza virion contains segments of viral RNA bound to four different proteins. Retroviral RNA is bound to a nucleocapsid protein which in turn is enclosed in a capsid, while togavirus RNA is located within an icosahedral shell.

Until recently, it was believed that the genome of all other known enveloped DNA and RNA viruses is always associated with one or more viral proteins. This belief may be changed by the isolation, from a solar saltern in Trapani, Italy, of a virus that infects the archaeal species Halorubrum. Salterns are multi-pond systems in which sea water is evaporated to produce salt. In such hypersaline envrionments, Archaea predominate, and about 20 archaeal viruses have been isolated from these locations.

The virus isolated from the Italian saltern is called Halorubrum pleomorphic virus-1, or HRPV-1. Biochemical analyses of the virion show that it is composed of lipids and two structural proteins, VP3 and VP5. The genome is a circular ssDNA about 7 kb in length with nine open reading frames. The virion architecture is unique: it is composed of a flexible membrane (hence the designation pleomorphic) that contains external spikes of the VP4 protein, and is lined on the interior with VP3. The viral DNA is apparently not bound to any proteins in the virions.

At the upper left is my depiction of the appearance of HRPV-1. The diagram was produced by deleting the internal proteins and nucleic acid of a simple retrovirus and replacing these with a ssDNA genome. The HRPV-1 VP4 spikes and the internal VP3 proteins are present, but no proteins are bound to the viral genome. Whether or not the VP4 spikes are oligomeric as shown is unknown.

Most enveloped viruses acquire their lipid membrane by budding from the host cell, and a similar mechanism could account for the formation of HRPV-1 virions. In the absence of a nucleoprotein, it is not clear how the viral genome would be specifically incorporated into the budding envelope. Another condundrum is how the virions would pass through the proteinaceous layer that covers the archaeal host cell.

Whether HRPV-1 is representative of a new kind of virus lacking nucleocapsid protein will be revealed by the study of other pleomorphic enveloped viruses. Candidates include bacterial viruses that infect mycoplasmas, and another pleomorphic haloarchaeal virus isolated from a different Italian saltern, Haloarcula hispanica pleomorphic virus 1.

Pietila, M., Laurinavicius, S., Sund, J., Roine, E., & Bamford, D. (2009). The Single-Stranded DNA Genome of Novel Archaeal Virus Halorubrum Pleomorphic Virus 1 Is Enclosed in the Envelope Decorated with Glycoprotein Spikes Journal of Virology, 84 (2), 788-798 DOI: 10.1128/JVI.01347-09