We provide here, for the first time, insights into the initial infection stages of a large spindle-shaped archaeal virus and explore the following life cycle events. Our observations suggest that Sulfolobus monocaudavirus 1 (SMV1) exhibits a high adsorption rate and that virions adsorb to the host cells via three distinct attachment modes: nosecone association, body association, and body/tail association. In the body/tail association mode, the entire virion, including the tail(s), aligns to the host cell surface and the main body is greatly flattened, suggesting a possible fusion entry mechanism. Upon infection, the intracellular replication cycle lasts about 8 h, at which point the virions are released as spindle-shaped tailless particles. Replication of the virus retarded host growth but did not cause lysis of the host cells. Once released from the host and at temperatures resembling that of its natural habitat, SMV1 starts developing one or two tails. This exceptional property of undergoing a major morphological development outside, and independently of, the host cell has been reported only once before for the related Acidianus two-tailed virus. Here, we show that SMV1 can develop tails of more than 900 nm in length, more than quadrupling the total virion length.
IMPORTANCE
Very little is known about the initial life cycle stages of viruses infecting hosts of the third domain of life,Archaea. This work describes the first example of an archaeal virus employing three distinct association modes. The virus under study, Sulfolobus monocaudavirus 1, is a representative of the large spindle-shaped viruses that are frequently found in acidic hot springs. The results described here will add valuable knowledge about Archaea, the least studied domain in the virology field.A rchaeal viruses constitute an integral part of the virosphere, and they are a ubiquitous feature of archaeal existence. Many Archaea are recognized as extremophiles, inhabiting extreme environments such as hot springs and solar salterns in high abundance (1, 2). Thus, viruses infecting extremophilic Archaea can be considered key players in the complex population dynamics in these environments. Through host infection, viruses can influence microbial diversity by introducing genetic variation, affect host cell physiology, and directly kill their hosts by cell lysis (3, 4). However, we have only a rudimentary understanding of archaeal virus-host interactions. Much of the limited knowledge that we do have comes from studying the virus-host interplay in Sulfolobales species. Of the about 100 isolated archaeal viruses, more than 30% infect hyperthermophilic Sulfolobales hosts (5-7). Among these viruses, distinct characteristics are found: unique bottle, droplet, and spindle shapes; extracellular virion development; and unique proteins with unknown functions (8). These distinctive characteristics are likely to influence the interplay with their hosts and give rise to unique life cycle traits. This has proven true for the rodshaped Sulfolobus virus ...