Structural and Functional Studies of Archaeal
Viruses |
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Authors: | C Martin Lawrence Smita Menon Brian J Eilers Brian Bothner Reza Khayat Trevor Douglas and Mark J Young |
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Institution: | Departments of ‡Chemistry and Biochemistry and ¶Microbiology, Montana State University, Bozeman, Montana 59717 and the §Department of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037 |
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Abstract: | Viruses populate virtually every ecosystem on the planet, including the
extreme acidic, thermal, and saline environments where archaeal organisms can
dominate. For example, recent studies have identified crenarchaeal viruses in
the hot springs of Yellowstone National Park and other high temperature
environments worldwide. These viruses are often morphologically and
genetically unique, with genomes that show little similarity to genes of known
function, complicating efforts to understand their viral life cycles. Here, we
review progress in understanding these fascinating viruses at the molecular
level and the evolutionary insights coming from these studies.The last decade has seen resurgent interest in the study of viruses that
lie outside traditional agricultural and medical interests. One reason is the
growing appreciation of the enormous abundance and impact of viruses on the
greater biosphere. For example, the oceans are thought to contain
~1031 viruses, a truly astronomical number
(1), making viruses the most
abundant biological entities in this ecosystem, where they catalyze turnover
of 20% of the oceanic biomass per day
(1). Remarkably, the virosphere
has now been shown to extend to almost every known environment on earth,
including the extreme acidic, thermal, and saline environments where archaeal
organisms can be dominant. Thus, because of their abundance and variety,
viruses are now thought to represent the greatest reservoir of genetic
diversity on the planet
(2).A second reason to study archaeal viruses is a growing appreciation for the
roles viruses play in evolution. Remarkably with >500 cellular genomes
sequenced to date, most show a significant amount of viral or virus-like
sequence within their genome, further evidence that viruses play a central
role in horizontal gene transfer and help drive the evolution of their hosts.
Roles for viruses in cellular evolution are also being considered. Current
hypotheses contend that viruses have catalyzed several major evolutionary
transitions, including the invention of DNA and DNA replication mechanisms
(3), the origin of the
eukaryotic nucleus (4), and
thus a role in the formation of the three domains of life. In addition, there
is also considerable interest in viral genesis and evolution in and of itself.
To evaluate these hypotheses and to analyze evolutionary relationships among
viruses, knowledge of viruses infecting the archaea is essential, yet these
viruses are vastly understudied. Finally, interest in archaeal viruses stems
also from the exceptional molecular insight viruses have traditionally
provided into host processes; archaeal viruses are certain to provide new
insights into the molecular biology of this poorly understood domain of
life.Pioneering studies by Wolfram Zillig et al.
(5) identified the first
archaeal viruses. Although initial studies suggested that viruses infecting
the euryarchaea (principally halophiles and methanogens) were similar to
head-tail bacteriophage, studies of viruses infecting the hyperthermophilic
crenarchaea revealed morphologies suggesting new viral families. Indeed, work
by several laboratories has led to the identification of seven new viral
families infecting the crenarchaea, the Globuloviridae, Guttaviridae,
Fuselloviridae, Bicaudaviridae, Ampullaviridae, Rudiviridae, and
Lipothrixviridae ()
(6,
7), with
STIV3
(8) and STSV1
(9) awaiting assignment. All of
these viruses contain double-stranded DNA genomes ranging in size from 13.7 to
75.3 kilobase pairs, encoding 31–74 ORFs. Although many package a
circular genome, the filamentous Lipothrixviridae and rod-shaped Rudiviridae
are notable exceptions and are the only viruses in any domain known to
encapsidate linear double-stranded DNA. Although most crenarchaeal viruses are
enveloped, the Rudiviridae are devoid of lipid, and with the
exception of the Fuselloviridae, they employ a lytic life cycle,
although only STIV and ATV (Bicaudaviridae) are known to cause cell
lysis
(11).4Open in a separate windowMorphological diversity in crenarchaeal viruses. A,
clockwise, beginning at upper left: STIV
(8), a PSV-like virus,
Sulfolobus neozealandicus droplet-shaped virus (SNDV)
(47), SSV1
(48), STSV1
(9), an ATV-like virus, an SIRV
virus, and S. icelandicus filamentous virus (SIFV)
(10). Micrographs of SIRV,
PSV-like, and ATV-like viruses from Yellowstone National Park are the courtesy
of M. J. Y. Other panels are reproduced, with permission, from Refs.
8–10,
47, and
48. B, cryoelectron
microscopy reconstruction of the STIV particle
(8) showing a cutaway view
(20) of the T = 31
icosahedral capsid with turret-like projections that extend from each of the
5-fold vertices. Portions of the protein shell (blue) and inner lipid
layer (yellow) have been removed to reveal the interior.The exceptional morphology of these viruses has been reviewed
(6,
7) and thus is only summarized
here (). For the
rod-shaped Rudiviridae, plugs are seen at both ends, from which three
short tail fibers emanate, whereas the Lipothrixviridae show mop- or claw-like
structures at both ends (6).
Similarly, the non-tailed icosahedral viruses, STIV and euryarchaeal SH1, have
large turrets or spikes that project from the surface
(8,
12). In each case, these
structures are thought to facilitate virus-host interactions. In contrast,
other crenarchaeal viruses utilize a fusiform or lemon-shaped virion, a
morphology unique to archaeal viruses. These fusiform viruses generally
contain tail fibers or an extended tail on one end that is also involved in
host recognition. For ATV, however, nascent particles are devoid of tails when
released from the host (13).
Remarkably, extended tails develop at both ends of the virion in an
extracellular maturation process. Finally, Acidianus bottle-shaped
virus (Ampullaviridae) shows an exceptional morphology that differs in its
basic architecture from any known virus. |
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