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A Unique Virus Release Mechanism in the Archaea

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A Unique Virus Release Mechanism in the Archaea A unique virus release mechanism in the Archaea Ariane Bizea, Erik A. Karlssonb, Karin Ekefja¨ rdb, Tessa E. F. Quaxa, Mery Pinaa, Marie-Christine Prevostc, Patrick Forterrea, Olivier Tenaillond, Rolf Bernanderb, and David Prangishvilia,1 aBiologie Mole´culaire du Ge`ne chez les Extreˆmophiles and cPlate-Forme de Microscopie Ultrastructurale, Institut Pasteur, 25 rue du Docteur Roux, 75724 Paris cedex 15, France; bDepartment of Molecular Evolution, Evolutionary Biology Center, Uppsala University, Norbyva¨gen 18C, SE-752 36 Uppsala, Sweden; and dInstitut National de la Sante´et de la Recherche Me´dicale, Unite´722, Faculte´deme´ decine Xavier Bichat, Universite´Paris 7, 16 rue Henri Huchard, 75018 Paris, France Edited by Carl R. Woese, University of Illinois, Urbana, IL, and approved May 14, 2009 (received for review February 4, 2009) Little is known about the infection cycles of viruses infecting cells Results from Archaea, the third domain of life. Here, we demonstrate that the Growth Kinetics of SIRV2-Infected Cultures. OD and CFU values virions of the archaeal Sulfolobus islandicus rod-shaped virus 2 from uninfected and infected [multiplicity of infection (moi) Ϸ7] (SIRV2) are released from the host cell through a mechanism, involv- cultures of S. islandicus were monitored over time. The effects of ing the formation of specific cellular structures. Large pyramidal the virus were visible already 1.5 h after infection (Fig. 1). Whereas virus-induced protrusions transect the cell envelope at several posi- uninfected cultures pursued normal growth with a generation time tions, rupturing the S-layer; they eventually open out, thus creating of Ϸ13 h, the OD in infected cultures remained constant for Ϸ60 large apertures through which virions escape the cell. We also h (Fig. 1 A and C), after which growth resumed (Fig. 1C). During demonstrate that massive degradation of the host chromosomes this time period, the CFU values of uninfected controls remained occurs because of virus infection, and that virion assembly occurs in constant or increased slightly. In contrast, the CFU values de- the cytoplasm. Furthermore, intracellular viral DNA is visualized by creased dramatically in infected cultures, resulting in an Ϸ1,000- flow cytometry. The results show that SIRV2 is a lytic virus, and that fold reduction at6hafterinfection (Fig. 1B, 10.5 h). The CFU the host cell dies as a consequence of elaborated mechanisms orches- values also revealed growth of a minor cell population in infected trated by the virus. The generation of specific cellular structures for a cultures starting at early time points (Fig. 1D, from 15 h). This distinct step of virus life cycle is known in eukaryal virus-host systems growth was initially not detectable in the OD measurements (Fig. but is unprecedented in cells from other domains. 1C), because of the low concentration of this cell population at early MICROBIOLOGY time points. Thus, infection by SIRV2 has a pronounced effect on ͉ ͉ ͉ lysis virus factory hyperthermophile infection cycle the host cultures, preventing growth of a majority of the cells. To exclude the possibility that the results were linked to the high s for organisms belonging to the Bacteria and Eukarya, moi used, or to the specific growth conditions, similar experiments Amembers of the domain Archaea are infected by specific were performed at low moi (Ϸ10Ϫ3), at different temperatures viruses. The majority of archaeal viruses isolated so far contain (70 °C, 75 °C, and 78 °C), pHs (3.0 and 3.5), medium richnesses dsDNA as the genetic material and infect hyperthermophilic hosts (standard medium or 5-fold less rich medium), and with different from the phylum Crenarchaeota (1). The diversity and uniqueness host strains (S. islandicus strains KVEM10H3, HVE10/4, and of these viruses at both the morphological and genetic levels are LAL14/1). No significant differences were observed, indicating that such that they have been classified into 7 viral families (2). The the effects occurred independently of these parameters. knowledge on the biology of this exceptional group of viruses is still The cell population growing in the presence of SIRV2 consisted limited, partly because of the unique genetic content: very few genes of cells completely resistant to SIRV2 infection, not producing any have detectable functions or homologs in the databases (3). detectable infectious virions nor carrying the SIRV2 genome (SI In particular, little is known about relationships of crenarchaeal Text and Fig. S1). This was consistent with the observation that the viruses with their hosts. Except for a few isolated cases (4–6), it is SIRV2 genome does not integrate into the host chromosome (11), generally presumed that these viruses persist in the host cell in a and excluded the possibility that SIRV2 established a carrier state carrier state, a nonlytic relationship in which virions are continu- relationship with its host. The high initial proportion of resistant ously secreted by the still-dividing cells (7). However, the classifi- cells suggested that specific mechanisms could be involved in their cation of crenarchaeal viruses as chronic is based on indirect generation, in addition to random mutations, such as CRISPR- experimental evidence, such as a lack of optical density (OD) related mechanisms (18). decrease and absence of cellular debris in infected cultures (e.g., 8, 9). Detailed characterization of the infection cycle and the carrier Flow Cytometry Analysis of Infected Cells over Time. The cell size and state has not been specifically addressed in the scarce reports on intracellular DNA content in uninfected and SIRV2-infected cul- crenarchaeal host-virus interactions (see e.g., 10). tures (moi Ϸ10) over time were monitored by flow cytometry (Fig. To study the nature of host-virus relationships in crenarchaea, we 2, Fig. S2, and Fig. S3). selected the nonenveloped, rod-shaped virus SIRV2 and its hyper- The relative lengths of the S. islandicus cell cycle periods in the thermophilic and acidophilic host, Sulfolobus islandicus. SIRV2, control cultures were found to be similar to those of other Sulfolo- originally described as a carrier state, nonlysogenic virus (11), bus species (16, 19), with the post-replicative phase occupying a Rudiviridae belongs to a common crenarchaeal virus family, the (9, large fraction of the generation time (68%, Fig. S4). Based on 11, 12, 13, 14), and contains a linear 35.5-kb dsDNA genome (15). comparison of the flow cytometry fluorescence (DNA content) The host belongs to a well characterized crenarchaeal genus, Sulfolobus (16, 17), from which also other viruses are known (2). We describe detailed in vivo effects of the virus on its host and, Author contributions: A.B., O.T., R.B., and D.P. designed research; A.B., E.A.K., K.E., T.E.F.Q., unexpectedly, demonstrate that SIRV2 is a cytocidal, lytic virus. M.P., and M.-C.P. performed research; A.B., E.A.K., M.-C.P., P.F., O.T., R.B., and D.P. analyzed Remarkably, a unique virus release mechanism was encountered data; and A.B., R.B., and D.P. wrote the paper. during the characterization, involving the generation of pyramidal The authors declare no conflict of interest. structures that, by opening out, cause local disruption of the cell This article is a PNAS Direct Submission. envelope and allow virion escape. In addition, intracellular viral 1To whom correspondence should be addressed. E-mail: [email protected]. DNA was visualized by flow cytometry, and the technique was also This article contains supporting information online at www.pnas.org/cgi/content/full/ used to demonstrate chromosome degradation in infected cells. 0901238106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0901238106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 25, 2021 Fig. 1. Impact of SIRV2 infection on the growth kinetics of S. islandicus cultures. Cul- tures infected at a moi of Ϸ7 (filled circles, continuous line) and uninfected cultures (empty circles, dotted lines), were launched in triplicates. Averages of the replicates Ϯ1SDare shown. The vertical arrows in A and B corre- spond to virus addition (4.5 h). (A)OD595 nm, detail of the first hours. (B) Log transformation of the CFU titres, detail of the first hours. (C) OD595 nm over the entire time course. (D) Log transformation of the CFU titers over the entire time course. signals with those from the sequenced genomes of S. acidocaldarius decrease over time. In infected cultures, chromosome-less cells and S. solfataricus, the genome size was estimated to Ϸ2.6Mb(Fig. began to accumulate in the first hours, and after 5 h, the percentage S5). The average cell size (Fig. 2A Left and Fig. S3) progressively was Ϸ40%, confirming that significant degradation occurred before decreased when the cultures approached stationary phase. In the virion release (at Ϸ8–10 h, see below) and, at 11 h, Ͼ80% of the infected cultures (Fig. 2B Left), a cell size increase initially occurred cells were chromosome-less. Subsequent degradation occurred at a in part of the cell population, evident as an extension of the lower rate and finally reached 97%, confirming that genome distribution toward the right (6–8 h). Subsequently, the average cell degradation occurred in most cells. size gradually decreased over time. The intracellular amount of SIRV2 DNA (Fig. 3 B and D) The DNA content distributions of the control cultures (Fig. 2A increased gradually and reached a maximum after Ϸ8 h, followed Right and Fig. S2) were typical for exponentially growing Sulfolobus by a large decrease up until 14 h. The initial increase presumably cells (19), with a majority of the cells containing 2 chromosomes. In corresponded to viral DNA replication, and the decrease to virus the infected cultures (Fig. 2B Right), cells with a very low DNA release, indicating a latent period of Ϸ8–10 h.
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