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1. Intraspecific antagonism through viral toxin encoded by chronic Sulfolobus spindle-shaped virus

   https://doi.org/10.1098/rstb.2020.0476  

   DeWerff, Samantha J.; Zhang, Changyi; Schneider, John; Whitaker, Rachel J. (January 2022, Philosophical Transactions of the Royal Society B: Biological Sciences)

   Virus–host interactions evolve along a symbiosis continuum from antagonism to mutualism. Long-term associations between virus and host, such as those in chronic infection, will select for traits that drive the interaction towards mutualism, especially when susceptible hosts are rare in the population. Virus–host mutualism has been demonstrated in thermophilic archaeal populations where Sulfolobus spindle-shaped viruses (SSVs) provide a competitive advantage to their host Sulfolobus islandicus by producing a toxin that kills uninfected strains. Here, we determine the genetic basis of this killing phenotype by identifying highly transcribed genes in cells that are chronically infected with a diversity of SSVs. We demonstrate that these genes alone confer growth inhibition by being expressed in uninfected cells via a Sulfolobus expression plasmid. Challenge of chronically infected strains with vector-expressed toxins revealed a nested network of cross-toxicity among divergent SSVs, with both broad and specific toxin efficacies. This suggests that competition between viruses and/or their hosts could maintain toxin diversity. We propose that competitive interactions among chronic viruses to promote their host fitness form the basis of virus–host mutualism. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. 

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2. Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions

   https://doi.org/10.1038/s41396-020-00870-1  

   Berg, Maureen; Goudeau, Danielle; Olmsted, Charles; McMahon, Katherine D.; Yitbarek, Senay; Thweatt, Jennifer L.; Bryant, Donald A.; Eloe-Fadrosh, Emiley A.; Malmstrom, Rex R.; Roux, Simon (June 2021, The ISME Journal)

   Abstract Temperate phages are viruses of bacteria that can establish two types of infection: a lysogenic infection in which the virus replicates with the host cell without producing virions, and a lytic infection where the host cell is eventually destroyed, and new virions are released. While both lytic and lysogenic infections are routinely observed in the environment, the ecological and evolutionary processes regulating these viral dynamics are still not well understood, especially for uncultivated virus-host pairs. Here, we characterized the long-term dynamics of uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake (Trout Bog Lake, TBL). As no GSB virus has been formally described yet, we first used two complementary approaches to identify new GSB viruses from TBL; one in vitro based on flow cytometry cell sorting, the other in silico based on CRISPR spacer sequences. We then took advantage of existing TBL metagenomes covering the 2005–2018 period to examine the interactions between GSB and their viruses across years and seasons. From our data, GSB populations in TBL were constantly associated with at least 2-8 viruses each, including both lytic and temperate phages. The dominant GSB population in particular was consistently associated with two prophages with a nearly 100% infection rate for >10 years. We illustrate with a theoretical model that such an interaction can be stable given a low, but persistent, level of prophage induction in low-diversity host populations. Overall, our data suggest that lytic and lysogenic viruses can readily co-infect the same host population, and that host strain-level diversity might be an important factor controlling virus-host dynamics including lytic/lysogeny switch. 

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3. Surface resistance to SSVs and SIRVs in pilin deletions of Sulfolobus islandicus

   https://doi.org/10.1111/mmi.14435  

   Rowland, Elizabeth F.; Bautista, Maria A.; Zhang, Changyi; Whitaker, Rachel J. (December 2019, Molecular Microbiology)

   Abstract Characterizing the molecular interactions of viruses in natural microbial populations offers insights into virus–host dynamics in complex ecosystems. We identify the resistance ofSulfolobus islandicustoSulfolobusspindle‐shaped virus (SSV9) conferred by chromosomal deletions of pilin genes,pilA1andpilA2that are individually able to complement resistance. Mutants with deletions of bothpilA1andpilA2or the prepilin peptidase, PibD, show the reduction in the number of pilins observed in TEM and reduced surface adherence but still adsorb SSV9. The proteinaceous outer S‐layer proteins, SlaA and SlaB, are not required for adsorption nor infection demonstrating that the S‐layer is not the primary receptor for SSV9 surface binding. Strains lacking both pilins are resistant to a broad panel of SSVs as well as a panel of unrelatedS. islandicusrod‐shaped viruses (SIRVs). Unlike SSV9, we show thatpilA1orpilA2is required for SIRV8 adsorption. In sequencedSulfolobusstrains from around the globe, one copy of eachpilA1andpilA2is maintained and show codon‐level diversification, demonstrating their importance in nature. By characterizing the molecular interactions at the initiation of infection betweenS. islandicusand two different types of viruses we hope to increase the understanding of virus–host interactions in the archaeal domain. 

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4. Effector-mediated plant–virus–vector interactions

   https://doi.org/10.1093/plcell/koac058  

   Ray, Swayamjit; Casteel, Clare L (February 2022, The Plant Cell)

   Abstract Hemipterans (such as aphids, whiteflies, and leafhoppers) are some of the most devastating insect pests due to the numerous plant pathogens they transmit as vectors, which are primarily viral. Over the past decade, tremendous progress has been made in broadening our understanding of plant–virus–vector interactions, yet on the molecular level, viruses and vectors have typically been studied in isolation of each other until recently. From that work, it is clear that both hemipteran vectors and viruses use effectors to manipulate host physiology and successfully colonize a plant and that co-evolutionary dynamics have resulted in effective host immune responses, as well as diverse mechanisms of counterattack by both challengers. In this review, we focus on advances in effector-mediated plant–virus–vector interactions and the underlying mechanisms. We propose that molecular synergisms in vector–virus interactions occur in cases where both the virus and vector benefit from the interaction (mutualism). To support this view, we show that mutualisms are common in virus–vector interactions and that virus and vector effectors target conserved mechanisms of plant immunity, including plant transcription factors, and plant protein degradation pathways. Finally, we outline ways to identify true effector synergisms in the future and propose future research directions concerning the roles effectors play in plant–virus–vector interactions. 

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5. Investigating Virus–Host Interactions in Cultured Primary Honey Bee Cells

   https://doi.org/10.3390/insects12070653  

   McMenamin, Alexander J.; Parekh, Fenali; Lawrence, Verena; Flenniken, Michelle L. (July 2021, Insects)

   Honey bee (Apis mellifera) health is impacted by viral infections at the colony, individual bee, and cellular levels. To investigate honey bee antiviral defense mechanisms at the cellular level we further developed the use of cultured primary cells, derived from either larvae or pupae, and demonstrated that these cells could be infected with a panel of viruses, including common honey bee infecting viruses (i.e., sacbrood virus (SBV) and deformed wing virus (DWV)) and an insect model virus, Flock House virus (FHV). Virus abundances were quantified over the course of infection. The production of infectious virions in cultured honey bee pupal cells was demonstrated by determining that naïve cells became infected after the transfer of deformed wing virus or Flock House virus from infected cell cultures. Initial characterization of the honey bee antiviral immune responses at the cellular level indicated that there were virus-specific responses, which included increased expression of bee antiviral protein-1 (GenBank: MF116383) in SBV-infected pupal cells and increased expression of argonaute-2 and dicer-like in FHV-infected hemocytes and pupal cells. Additional studies are required to further elucidate virus-specific honey bee antiviral defense mechanisms. The continued use of cultured primary honey bee cells for studies that involve multiple viruses will address this knowledge gap. 

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