Date Published: July 14, 2011
Publisher: Hindawi Publishing Corporation
Author(s): Jamie C. Snyder, Benjamin Bolduc, Mary M. Bateson, Mark J. Young.
A new type of viral-induced lysis system has recently been discovered for two unrelated archaeal viruses, STIV and SIRV2. Prior to the lysis of the infected host cell, unique pyramid-like lysis structures are formed on the cell surface by the protrusion of the underlying cell membrane through the overlying external S-layer. It is through these pyramid structures that assembled virions are released during lysis. The STIV viral protein c92 is responsible for the formation of these lysis structures. We searched for c92-like proteins in viral sequences present in multiple viral and cellular metagenomic libraries from Yellowstone National Park acidic hot spring environments. Phylogenetic analysis of these proteins demonstrates that, although c92-like proteins are detected in these environments, some are quite divergent and may represent new viral families. We hypothesize that this new viral lysis system is common within diverse archaeal viral populations found within acidic hot springs.
Compared to the viruses infecting organisms from the domains Bacteria and Eukarya, few viruses infecting archaeal organisms have been isolated and most are poorly understood in molecular detail. Most archaeal viruses are morphologically and genetically distinct from previously described viruses [1–4]. Sulfolobus turreted icosahedral virus (STIV) has emerged as a model system for examining archaeal virus replication and structure [5–15]. STIV was originally isolated from the Rabbit Creek thermal basin within Yellowstone National Park, (YNP) USA . The STIV virion contains a circular double-stranded (ds) DNA genome of 17,663 base pairs (bps) which encodes for 37 open reading frames (ORFs). The cryoelectron microscopy image reconstruction of STIV particles revealed a pseudo T = 31 capsid, an internal membrane, and turret-like projections extending from each of the virions fivefold axes . Structural analysis of the major capsid protein has suggested an evolutionary link between archaeal viruses and bacterial and eukaryotic viruses [7, 15].
Numerous metagenomic libraries from two geographically isolated thermal areas within YNP were used in this study. The first area is the Crater Hills thermal basin, containing an acidic (pH ~ 2.5) high-temperature (~82°C) hot spring (44.6532°N, 110.4847°W). The second thermal site is in the Nymph Lake area (44.7536°N, 110.7237°W) within Norris Geyser Basin in YNP and also contains acidic (pH ~ 3.5–4.5) and high-temperature (~91°C) hot springs. Over the course of four years we have produced a total of 39 metagenomic libraries from these two thermal areas within YNP. The metagenomes are enriched for either viral or cellular sequences by methods previously described (, B. Bolduc, F. F. Roberto, M. Lavin, and M. J. Young, manuscript in prep.).
The communities present in the acidic hot springs within YNP are dominated by archaeal organisms [21, 24, 25]. The unique viral lysis system described for STIV [12, 14] and SIRV2 [18–20] appears within the archaeal viral community associated within YNP acidic hot springs. By comparing STIV c92 and homologues in rudiviral genomes against our YNP viral and cellular metagenomic databases, we found 70 contigs coding for protein sequences that represent closely related proteins.
Little is known about the viruses that infect organisms from the domain Archaea. Previously, it had been suggested that most archaeal viruses were nonlytic primarily due to the harsh conditions that many of these organisms inhabit and to the presence of integrase-like genes in many of the viral genomes. STIV was the first lytic crenarchaeal virus discovered , and SIRV2 was subsequently found to be lytic as well . Homologous viral proteins from STIV and SIRV2 were discovered to be responsible for the formation of the unique pyramid lysis structures present on the Sulfolobus cellular membrane prior to viral-induced lysis [14, 18]. The presence of the viral-induced pyramid-like lysis structures on two unrelated viruses led us to investigate the prevalence of this type of viral lysis system in Archaea. We sought to determine the presence of c92-like proteins present in metagenomic datasets by comparing the sequenced STIV c92 protein to sequences collected from YNP.