Mutualistic Interactions of Viruses with Lower Eukaryotes

Mutualistic Interactions of Viruses with Lower Eukaryotes

Archives of Virology https://doi.org/10.1007/s00705-017-3686-5 REVIEW Enemies with benefts: mutualistic interactions of viruses with lower eukaryotes Shounak S. Jagdale1 · Rakesh S. Joshi1 Received: 8 July 2017 / Accepted: 6 November 2017 © Springer-Verlag GmbH Austria, part of Springer Nature 2018 Abstract Viruses represent some of the deadliest pathogens known to science. Recently they have been reported to have mutualistic interactions with their hosts, providing them direct or indirect benefts. The mutualism and symbiogenesis of such viruses with lower eukaryotic partners such as fungi, yeast, and insects have been reported but the full mechanism of interaction often remains an enigma. In many instances, these viral interactions provide resistance against several biotic and abiotic stresses, which could be the prime reason for the ecological success and positive selection of the hosts. These viruses modulate host metabolism and behavior, so both can obtain maximum benefts from the environment. They bring about micro- and macro- level changes in the hosts, benefting their adaptation, reproduction, development, and survival. These virus-host interactions can be bilateral or tripartite with a variety of interacting partners. Exploration of these interactions can shed light on one of the well-coordinated biological phenomena of co-evolution and can be highly utilized for various applications in agriculture, fermentation and the pharmaceutical industries. Introduction that results in the formation of a new species is a theory of evolution called symbiogenesis [2]. A fusion of the virus Viruses are intracellular parasites, with genomes capable with its host has been observed in interactions prevailing of directing their own replication. Classically they are clas- since ancient times, termed as viral symbiogenesis. Various sifed as non-cellular entities with an extrachromosomal mutualistic and symbiogenetic viruses of lower eukaryotes phase, without any essential function to their host [1]. Viral and their efects on host survival and adaptation are dis- pathogenicity is well studied through the various aspects of cussed here (Table 1). immunology, vaccine development, and genetic engineering. Recently, researchers have identifed mutualistic viruses of diferent organisms, but their replication and mechanism of Endophytic fungi and viruses interaction with the host still remains ambiguous. Discovery of such interactions has modifed the defnition of viruses, to Mycoviruses are dsRNA viruses that infect fungi. These account for mutualistic viruses, as ‘intracellular parasites, viruses are host dependent and their persistent infection with nucleic acids that are capable of directing their own leads to long-term transmission. In many cases, mycovi- replication, and are not cells’ [1]. ruses infect the host multiple times, thereby aiding the Mutualism is part of a very broad concept called symbio- host’s genetic variability, without causing any detrimental sis, which is an umbrella term that includes parasitism, com- efects [3]. Recently, symbiotic efects of mycoviruses on mensalism and mutualism – wherein both partners beneft various traits of endophytic fungi have been documented, from each other. The integration of two diferent organisms expounding a three-way symbiotic relationship amongst plants, fungi, and viruses [4]. In the case of a thermotol- erant panic grass, Dichanthelium lanuginosum, three-way Handling Editor: Robert H.A. Coutts. symbiosis has been described. The prime reason behind * Rakesh S. Joshi the growth of these plants in geothermal soils (65 °C) was [email protected]; [email protected] thought to be due to its association with a fungus named Curvularia protuberata [5]. However, the third partner 1 Institute of Bioinformatics and Biotechnology, Savitribai of this system was found to be a virus, the Curvularia Phule Pune University, Pune, Maharashtra 411007, India Vol.:(0123456789)1 3 S. S. Jagdale, R. S. Joshi thermal tolerance virus (CThTV) which is responsible for (TauD) leads to enhanced synthesis of osmolytes and conferring thermal tolerance to the plant [Figure 1]. The osmoprotectants, namely glycine betaine and taurine [7, spherical virus, with a diameter of 27 nm, contains 2 RNA 10, 11]. In addition, an elevated level of melanin due to segments of 2.2 and 1.8 kb. Each of the 2 strands contain 2 overexpression of scytalone dehydratase (SCD), provides ORFs. ORFs of RNA1, namely ORF1a and b, overlap each protection from extreme temperature and radiation [7, 12]. other and show sequence similarity to RNA-dependent Plants colonized by CThTV-infected C. protuberata show RNA polymerases (RdRp). RNA2 ORFs show no sequence constitutive overexpression of osmolytes when compared similarity with sequences currently available. The verti- to normal plants [6]. However, the exact mechanism of this cal transmission of the virus takes place through conidi- virus mediated thermal tolerance in plants is still unclear. ospores [6]. Virus infected C. protuberata show a two-fold It was reported that C. protuberata could colonize increase in the expression of trehalose phosphate synthase various plants such as Oryza sp., Triticum sp., Solanum (TPS) leading to increased levels of an osmoprotectant - lycopersicum and Cucurbita pepo [13]. In S. lycoper- trehalose - that maintains protein and membrane integrity sicum, thermal tolerance is observed when associated under environmental stress conditions [7, 8]. Furthermore, with CThTV infected C. proturberata [6, 14]. Thus, this metabolic overexpression of mannitol, a potential osmo- mechanism of virus infection-mediated thermal protection protectant, is also observed in the hyphae [9]. Similarly, can be applied to other plants for the development of abi- upregulation of the homologs of betaine aldehyde dehy- otic stress tolerance. drogenase (BadH) and taurine catabolism dioxygenase Fig. 1 Three-way symbiotic relationship amongst plant, Infection of CThTV C. proturberta endophytic fungus and a virus. D. lanuginosum shows enhanced thermal tolerance [65 °C]. This thermal tolerance is acquired due to the presence of a dsRNA virus CThTV resid- ing within an endophytic fungus C. proturberta Increased Thermo tolereance D. lanuginosum 1 3 Mutualism between viruses and lower eukaryotes Mutualistic viruses of yeast ORF which encode the killer pre-protoxin. Satellite viruses parasitize the helper virus for the production of their cap- Over the course of evolution, various organisms have devel- sid proteins [20]. Subsequently, the toxins produced, act on oped tactics to overcome competition. For example, yeasts sensitive yeast colonies in a two-step process: The frst step such as Saccharomyces cerevisiae, Ustilago maydis and is energy independent wherein, the toxin binds to the cell Zygosaccharomyces bailii utilize viral assisted toxin pro- wall receptor of sensitive yeast. K1 and K2 bind to β-1,6- duction to kill competing yeast colonies, and are thus called D-glucan, whereas K28 binds to α-1,3-mannoprotein [21, ‘killer yeast’ [15]. The totivirus Saccharomyces cerevisiae 22]. The second step is energy dependent, where the toxin virus L-A (ScV-L-A) present in the yeast helps in the sta- translocates to the cytoplasmic membrane and interacts with ble maintenance and replication of satellite viruses namely a secondary receptor [Figure 2]. For K1, this receptor is a S. cerevisiae virus M1 (ScV-M1), ScV-M2 or ScV-M28. GPI-anchored plasma membrane protein Kre1P and for K28, Infection of ScV-M1, ScV-M2 or ScV-M28 in S. cerevi- it is cellular HDEL receptor Erd2P [23, 24]. Interaction of siae results in the production of toxins, namely K1, K2 and K1 with Kre1P results in the formation of an ion channel, K28 [16–19]. ScV-L-A and ScV-M viruses show cytoplas- disrupting the cytoplasmic membrane [25–27]. K28, after mically-inherited, symptomless infection of killer yeast. binding to α-1,3-mannoprotein, is taken up by endocyto- ScV-L-A has 2 ORFs which encode gag and pol. The virus sis and is targeted to early endosomal compartments. From capsid protein consists of 120 copies of gag and 2 copies of there, it enters the cell cytosol through the secretory pathway a gag-pol fusion protein. The satellite viruses have only 1 and blocks cellular DNA synthesis, arresting the cells in early S phase [28]. Sensitive yeast ScV-L-A K1, K2 or ScV-M K28 toxin Erd2P Kre1P Ion-channel formation in the ScV-M β-1-6 D-Glucan cytoplasm by K1 and toxin α-1-3- mannoprotein K28 endocytosis Block in DNA synthesis by K28 toxin Killer yeast Fig. 2 Killer yeast mechanism of action. Killer yeast harbour the sat- lowed by binding to plasma membrane receptors Kre1P and Erd2P. ellite M viruses which parasitize the helper L-A virus for coat pro- Once inside the sensitive yeast cell, K1 toxin results in ion channel teins. M viruses then produce the toxins K1, K2 or K28 which act formation in the cytoplasmic membrane and K28 translocates to the on the sensitive yeast colonies in a 2-step process. Toxins frst bind nucleus blocking DNA synthesis to cell wall receptors β-1,6-D glucan and α-1,3-manonprotein fol- 1 3 S. S. Jagdale, R. S. Joshi It is critical for the killer yeast to be immune to these tox- hemocytes, creating favorable conditions for the survival of ins. Killer yeast immunity against these toxins involves the wasp eggs and larval development [39, 40]. The Cotesia con- K1 toxin precursor, which acts as a competitive inhibitor of gregrata bracovirus (CcBV) genome contains 156 genes; 27 the active toxin by saturating the plasma membrane receptor. genes encoding protein tyrosine phosphatases and 6 for pro- In the case of K28 toxin, the active toxin taken up by killer teins with ankyrin repeat motifs from the IκB family, which cells binds to the pre-protoxin present in the cytosol. This inhibit the immune responses. Four genes code for cysteine- protein complex is then ubiquitinated and degraded by the rich cysteine knot motif proteins, similar to the teratocyte proteasome machinery [29]. Both helper and satellite viruses secreted protein 14 (TSP 14) which inhibits the translation are dependent on the expression of several yeast chromo- of storage proteins in the hosts, resulting in developmental somal genes.

View Full Text

Details

  • File Type
    pdf
  • Upload Time
    -
  • Content Languages
    English
  • Upload User
    Anonymous/Not logged-in
  • File Pages
    10 Page
  • File Size
    -

Download

Channel Download Status
Express Download Enable

Copyright

We respect the copyrights and intellectual property rights of all users. All uploaded documents are either original works of the uploader or authorized works of the rightful owners.

  • Not to be reproduced or distributed without explicit permission.
  • Not used for commercial purposes outside of approved use cases.
  • Not used to infringe on the rights of the original creators.
  • If you believe any content infringes your copyright, please contact us immediately.

Support

For help with questions, suggestions, or problems, please contact us