Disclaimer: This dissertation has been written by a student and is not an example of our professional work, which you can see examples of here.

Any opinions, findings, conclusions, or recommendations expressed in this dissertation are those of the authors and do not necessarily reflect the views of UKDiss.com.

Host Recognition and Cyanophage Adsorption

Info: 4377 words (18 pages) Dissertation
Published: 18th May 2020

Reference this

Tags: Biology

Host Recognition and Cyanophage Adsorption

The first step in the interaction of cyanophages and cyanobacterial hosts involves cyanophages use their receptor-binding proteins to recognise cyanobacterial cell surface receptor molecules for adsorption to the surface of host cells. In gram-negative bacteria includes cyanobacteria, the cell wall is composed of the cytoplasmic membrane, the peptidoglycan layer, and the outer membrane [1]. Lipopolysaccharides (LPS) on the outer membrane are the most common phage receptor [2], which are consisting of a lipid A, inner and outer core oligosaccharides, and an O-antigen [3]. It was first discovered that the LPS of Anacystis nidulans (strains KM, 6301, 6311, and 6908), Anacystis IUCC 1549, Synechococcus (stain 6910, 6312), Coccochloris peniocystis (strains 6307, 6603), Synechococcus elongatus 6907, and Microcystis aeruginosa 6911 can all inactivates the infection of the AS-1 at various degree [4]. Although the inactivation of AS-1 infection can be stopped by adding TMN buffer, no reactivation of AS-1 infection was observed [4]. Furthermore, the lipid A region of the A. nidulans LPS showed no capacity of inactivation towards AS-1 infection [4]. On the other hand, the O-antigen determines the susceptibility of Anabaena speciesinfection by cyanophage A-1(L) and A-4(L), which O-antigen constitutes the receptor to which the phages adsorb [5]. Anabaena speciesgenes rfbP and rfbZ are response for the O-antigen assembly in LPS, while the Tn5 insertional inactivation of these genes abolished and altered the synthesis of O-antigen, respectively. Such inactivation led to the resistance to A-1(L) and A-4(L) in Anabaena species [5].

Cyanophage Host-Recognition Proteins

The adsorption of the cyanophage to the cell wall of cyanobacterial host is through the distal portion of the tails [6]. Among the predicted A-1(L) tail proteins, ORF35 and ORF36 encode proteins responsible for the adsorption onto the cell surface of Anabaena 7120 [7]. The function of A-1(L) orf35 protein was not identified, but several homologous proteins of orf35 was found in other phages, such as Nostoc phage N1 orf32 protein and A-4(L) orf24 protein, which were both predicted to be tail fibre proteins [8; 9]. The A-1(L) orf36 was identified as a tail collar protein which function as the receptor-binding protein that interacts with the LPS, also known as the LPS-interacting protein (LIP) [7]. The His-X-His pair of A-1(L) LIP was suggested to facilitate the trimeric formation of the tail fibre proteins (orf35)[7], like gp12 and gp37 in T4, which responsible for the reversible binding to the O-antigen of host LPS during the initial step of the adsorption [10]. The orf35 protein was proposed responsible for the irreversible binding to a different site (such as a minor host outer membrane proteins or other receptors on the host cell surface) during the second step of the adsorption [7].

On the cyanophage Syn5, a single “horn”-like protein was identified on the opposite end of the capsid from the tail, which was attached to the vertex at the final step of capsid assembly [11]. The horn is an elongated fibrous protrusion with a length of about 50 nm, a bottom width of 10 nm, and a tip that tapers to 2-5 nm [12]. The “horn” was hypothesised as an additional recognition structure comprised of two highly antigenic proteins (a 48 kDa gp53 and a 65 kDa gp54) encoded by the cyanophage Syn5 [12]. The gp53 was observed as the shaft protein of the “horn”, and the gp54 was observed forms the tip of the “horn” [13]. The similar head appendage structure was also observed on the vertex opposite the tail of the Caulobacter crescentus phages Cb13 and CbK, which the head appendage wrap tightly around the host flagellum [14]. Although anti-gp53 and anti-gp54 antibodies showed no inactivation of the Syn5 infectivity toward Synechococcus  WH8109 and suggests that the horn may not be needed for the Syn5 infection toward WH8109 [13]. The “horn” may still serve as a host recognition structure to a host other than WH8109. Also, the antibodies were raised against recombinant “horn” proteins which were not in their native forms, the antibodies may bind to the “horn” epitopes that is different to the recognition site of the “horn” structure.

Also on the cyanophage Syn5, a “knob”-like protein gp55 protruding from the capsid surface was identified and appears to be responsible for the stabilisation of the capsid structure of the mature Syn5 [15]. In addition, the Blast sequence analysis indicated that the gp55 shares similarities with a region of the TonB receptor belongs to the porin superfamily [15]. The TonB receptors of the gram-negative bacteria are outer membrane proteins that responsible for the signal sensing [16; 17], which indicates gp55 might function as a weak host cell surface recognition protein or a host cell surface receptor mimic protein. Considering these cyanophage-cyanobacterial populations locate in harsh oligotrophic oceanic environment [18], such surface proteins (“horn”-like proteins gp53 and gp54, and “knob”-like protein gp55) might facilitate the binding of cyanophage to non-host particles [19] to aid in travelling to dense host populations in nutrient-rich waters.

Light Dependency of Cyanophage Adsorption

 In nature, cyanobacteria undergo diel light-dark cycles, which have significant impacts on the cyanophage life cycle. During the adsorption step, some cyanophages exhibited a diurnal adsorption rhythm, a light-dependent adsorption pattern [20; 21; 22]. Early laboratory studies showed that Synechococcus cyanophage AS-1 demonstrated such light-dependent adsorption mode toward Synechococcus PCC6301. Under normal light conditions, the adsorption rate of AS-1 was 80%, and the adsorption rate of AS-1 in the dark was reduced to 40% without influencing the adsorption rapidness [20]. However, within 10 to 15 minutes after reillumination, the decreased adsorption rate of AS-1 returned to the normal level [20]. Such strong light-dependent influence has also been found on the infection of AS-1 towards Synechococcus elongatus PCC7942 at the level of adsorption [21]. Another Synechococcus cyanophage S-PM2 demonstrated a light-dependent pattern in both the adsorption rate and the adsorption rapidness toward Synechococcus WH7803, which the adsorption rate was decreased from 90% to 15% and the adsorption rapidness was slowed from 45 minutes to 3 hours in the dark when compared to in the light [22]. The light dependency of S-PM2 was also varies from host to host, i.e., lower light dependency towards Synechococcus strain BL161 than strain WH7803 [22]. Other Synechococcus cyanophages, such as S-BnM1, S-BM3, S-BP3, S-MM1, S-MM4, S-MM5, S-PWM1, and S-PWM3, all displayed a light-dependent adsorption pattern [22]. Moreover, Prochlorococcus cyanomyoviruses P-HM1, P-HM2, P-SSM2 and cyanopodoviruses P-SSP7, P-GSP1 displayed various light-dependent adsorption as well as light-dependent replication patterns [23]. First, P-HM2 and P-HM1 did not adsorb to host cells in the dark; Second, P-SM2 adsorbed to host cells in the dark but with a lower rate when compared to the adsorption rate in the light, and P-SM2 do not replicate in the dark; Third, P-SSP7 and P-GSP1 both adsorbed to host cells and also replicate in host cells in the dark [23]. The light dependency adsorption of cyanophages has been explained as due to the light-sensitive conformational alterations in host cell surface receptors or in cyanophage tail fibers that be triggered by light [22].

 Effects of different wavelengths on the cyanophage adsorption has also been examined.  No noticeable difference was observed in the phage adsorption rate under blue, green, or yellow light illuminations when compared to under the white light, but the adsorption rate was significantly decreased under red light illumination. [22]. This may indicate a relationship between cyanophage adsorption rate and host photosynthetic metabolic pathways, i.e., the light absorption efficiency and the light harvest of phycoerythrin-rich marine cyanobacteria is higher under the blue and green light than under the red light [24; 25]. Also, the production of phycoerythrin is maximal in green light, and ensued by blue light in phycoerythrin producing cyanobacteria [26]. This wavelength-dependency raises the question of whether phage requires active photosynthesis in the host for the adsorption. While, cyanobacterial core photosystems I and II protein genes were identified in cyanophages [27; 28]; those genes were proposed to be functional in supplementing host photosynthesis during cyanophage infection and to increase viral fitness [29; 30; 31; 32]. However, the adsorption of cyanophage is independent from the host photosystem II-dependent electron flow and oxidative phosphorylation during the photosynthesis. This was demonstrated when treated Synechococcus WH7803 with photosystem II inhibitors carbonyl cyanide m-chlorophenyl hydrazone (CCCP) and 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) before cyanophage S-PM2 adsorption, and no influence of S-PM2 adsorption was observed [22; 23].

Salt Concentration Dependency of Cyanophage Adsorption

 The adsorption of cyanophages is also depend on the salt concentration in the culture medium. The adsorption kinetics of AS-1 to the host Synechococcus cedrorum followed the first-order reaction. When the NaCl concentration increased from 0 to 0.1M, the adsorption rate of AS-1 increased from 51% to 85% [33].Moreover, a 10-fold increase in the concentration of Na+ can counteract the effects of darkness and restore the adsorption rate of AS-1 to the level obtained under illumination, although no evidence shows that Na+ and illumination affect AS-1 adsorption in the same mechanism [20]. The Na+ increasing-induced increased AS-1 adsorption rate was observed on a broad range of hosts (includes Anacystis nidulans stains KM, 6301, 6311, 6908, Anacystis IUCC 1549, Synechococcus stain 6910, 6312, Coccochloris peniocystis stains 6307, 6603, Synechococcus elongatus strain 6907, and Microcystis aeruginosa strain 6911) [4]. However, some Synechococcus cyanophage demonstrated a adsorption pattern that was independent of the presence of Na+ [6]. The Na+ dependency of the cyanophage adsorption rate can be explained as being due to the salt cation-induced changes or neutralisation of the ionic level at the host cell surface.

Stages During Cyanophage Adsorption

 The adsorption of cyanophage P-SSP7 to its host Prochlorococcus MED4 is a multiple-stage process: (1) free cyanophages which have not yet encountered host cells, with folded tail fibres adhered to themselves and pointing inward for protection; (2) cyanophages approach to the host cell surface spending a considerable amount of time attach their tail fibres parallelly to the host cell surface “exploring” to identify the host cellular receptor; (3) a leaning stage being indicative of pre-infection “walking” stage where viral tail fibres searching for host cell surface receptors; (4) once adhered to the receptor, some tail fibres appear to attach more firmly and to extend horizontally to enable the cyanophages to “stand” onto the host cell surface [34]. Each stages were identified with different orientations of P-SSP7 on the cell surface of MED4, parallel (~0 degree), leaning (~45 degree) and standing (~90 degree) [34]. For T4-like phages, the parallel stage is a well-studied attachment stage mediated by reversible and irreversible bindings of phage long and short tail fibres, respectively [10], and the “walking” stage has also been suggested for the T7 phage [35]. More interestingly, phages can also use their tail fibers to assess whether a cell is able to host a productive infection, which has been suggested for soil mycobacteriophages [36]. Conformational changes in P-SSP7 tail fibres during adsorption happen between the initial attachment (~23 minutes post infection) of P-SSP7 to MED4 to the start of genome translocation into the host (~86 minutes post infection) [34].

Cyanophages DNA Translocation

 In P-SSP7 cyanophages, after adsorption and achievement of a perpendicular “standing” orientation, which lead to a cascade structural alterations in the tail fibres and further in the tail-portal vertex complex, allowing the P-SSP7 adhere firmly to the cell surface for DNA translocation [34]. This cascade structural alteration process can be used to ensure that the phage is in the proper orientation to efficiently deliver its viral DNA to the host through the an extensible tube [34]. Several core glycoproteins (gp14/15/16) of P-SSP7 have been hypothesised for the digestion of host envelope and the formation of a 500Å long, extensible channel from the tip of the tail and protect viral DNA during the translocation process [34; 37; 38; 39]. Such tubular features were also observed for ε15, T7, and syn5 phages during the infection of Salmonella, Escherichia coli and Synechococcus cells, respectively [11; 40; 41]. The portal vertex complex consists of the adaptor (gp11), nozzle (gp12), tail fibre (gp17), portal (gp8), and the dsDNA of viral genome [42]. Upon cyanophage binding to the cell surface and orients the portal vertex complex pointing perpendicular to the host cell surface, the DNA translocation initiates by first contact the host cell surface with the tail nozzle and extend the proximal segments of the tail fibres horizontally [34; 42]. Similar orientation adjustment has also been observed in T7 phages [40; 43; 44]. This tail fibre orientation adjustment leads the interaction among tail fibre, adaptor and the portal and further loosen the portal protein at the Q-rich motifs, thereby triggers the disassemble of the internal core proteins [42]. During this process, the DNA structure is also changed and may also facilitate the disassembly process [42]. The nozzle valve initially blocks the exit pathway of the DNA, but the conformational changes during this process cause the open of the nozzle valve, and then finally allow the cyanophage DNA to eject into the host freely [42].

 Some cyanophages, such as P-WMP4, depends on the host RNA polymerase to translocate their DNA. The DNA translocation of P-WMP4 follows a tree-step process: initial entry of the leading ~233 bp of the viral DNA by the internal force produced by DNA packing or the proton motive force; then the host RNA polymerase transcripts and leading the entry of ~16kb of cyanophage DNA; and the translocation of the remaining 24kb DNA is achieved by other cyanophage proteins that are expressed during the second step of DNA transfer [45]. Such DNA translocation mechanism has also been characterised in the T7 bacteriophage, which the DNA translocation utilise the E. coli RNA polymerase [46; 47; 48].


[1] E. Hoiczyk, and A. Hansel, Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182 (2000) 1191-9.

[2] J. Bertozzi Silva, Z. Storms, and D. Sauvageau, Host receptors for bacteriophage adsorption. FEMS Microbiol Lett 363 (2016).

[3] P. Durai, M. Batool, and S. Choi, Structure and Effects of Cyanobacterial Lipopolysaccharides. Mar Drugs 13 (2015) 4217-30.

[4] B. Samimi, and G. Drews, Adsorption of cyanophage AS-1 to unicellular cyanobacteria and isolation of receptor material from Anacystis nidulans. J Virol 25 (1978) 164-74.

[5] X. Xu, I. Khudyakov, and C.P. Wolk, Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120. J Bacteriol 179 (1997) 2884-91.

[6] M. Kim, and Y.K. Choi, A new Synechococcus cyanophage from a reservoir in Korea. Virology 204 (1994) 338-42.

[7] Z. Xiong, Y. Wang, Y. Dong, Q. Zhang, and X. Xu, Cyanophage A-1(L) Adsorbs to Lipopolysaccharides of Anabaena sp. Strain PCC 7120 via the Tail Protein Lipopolysaccharide-Interacting Protein (ORF36). J Bacteriol 201 (2019).

[8] T. Ou, X.Y. Liao, X.C. Gao, X.D. Xu, and Q.Y. Zhang, Unraveling the genome structure of cyanobacterial podovirus A-4L with long direct terminal repeats. Virus Res 203 (2015) 4-9.

[9] C. Chenard, J.F. Wirth, and C.A. Suttle, Viruses Infecting a Freshwater Filamentous Cyanobacterium (Nostoc sp.) Encode a Functional CRISPR Array and a Proteobacterial DNA Polymerase B. MBio 7 (2016).

[10] S.G. Bartual, J.M. Otero, C. Garcia-Doval, A.L. Llamas-Saiz, R. Kahn, G.C. Fox, and M.J. van Raaij, Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci U S A 107 (2010) 20287-92.

[11] W. Dai, C. Fu, D. Raytcheva, J. Flanagan, H.A. Khant, X. Liu, R.H. Rochat, C. Haase-Pettingell, J. Piret, S.J. Ludtke, K. Nagayama, M.F. Schmid, J.A. King, and W. Chiu, Visualizing virus assembly intermediates inside marine cyanobacteria. Nature 502 (2013) 707-10.

[12] W.H. Pope, P.R. Weigele, J. Chang, M.L. Pedulla, M.E. Ford, J.M. Houtz, W. Jiang, W. Chiu, G.F. Hatfull, R.W. Hendrix, and J. King, Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a “horned” bacteriophage of marine synechococcus. J Mol Biol 368 (2007) 966-81.

[13] D.A. Raytcheva, C. Haase-Pettingell, J. Piret, and J.A. King, Two novel proteins of cyanophage Syn5 compose its unusual horn structure. J Virol 88 (2014) 2047-55.

[14] R.C. Guerrero-Ferreira, P.H. Viollier, B. Ely, J.S. Poindexter, M. Georgieva, G.J. Jensen, and E.R. Wright, Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. Proc Natl Acad Sci U S A 108 (2011) 9963-8.

[15] P. Gipson, M.L. Baker, D. Raytcheva, C. Haase-Pettingell, J. Piret, J.A. King, and W. Chiu, Protruding knob-like proteins violate local symmetries in an icosahedral marine virus. Nat Commun 5 (2014) 4278.

[16] D.D. Shultis, M.D. Purdy, C.N. Banchs, and M.C. Wiener, Outer membrane active transport: structure of the BtuB:TonB complex. Science 312 (2006) 1396-9.

[17] O. Mirus, S. Strauss, K. Nicolaisen, A. von Haeseler, and E. Schleiff, TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biol 7 (2009) 68.

[18] M.B. Sullivan, J.B. Waterbury, and S.W. Chisholm, Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424 (2003) 1047-51.

[19] T. Sathaliyawala, M.Z. Islam, Q. Li, A. Fokine, M.G. Rossmann, and V.B. Rao, Functional analysis of the highly antigenic outer capsid protein, Hoc, a virus decoration protein from T4-like bacteriophages. Mol Microbiol 77 (2010) 444-55.

[20] C.S. Cseke, and G.L. Farkas, Effect of light on the attachment of cyanophage AS-1 to Anacystis nidulans. J Bacteriol 137 (1979) 667-9.

[21] C.C. Kao, S. Green, B. Stein, and S.S. Golden, Diel infection of a cyanobacterium by a contractile bacteriophage. Appl Environ Microbiol 71 (2005) 4276-9.

[22] Y. Jia, J. Shan, A. Millard, M.R. Clokie, and N.H. Mann, Light-dependent adsorption of photosynthetic cyanophages to Synechococcus sp. WH7803. FEMS Microbiol Lett 310 (2010) 120-6.

[23] R. Liu, Y. Liu, Y. Chen, Y. Zhan, and Q. Zeng, Cyanobacterial viruses exhibit diurnal rhythms during infection. Proc Natl Acad Sci U S A 116 (2019) 14077-14082.

[24] L.J. Ong, and A.N. Glazer, Phycoerythrins of marine unicellular cyanobacteria. I. Bilin types and locations and energy transfer pathways in Synechococcus spp. phycoerythrins. J Biol Chem 266 (1991) 9515-27.

[25] R.V. Swanson, L.J. Ong, S.M. Wilbanks, and A.N. Glazer, Phycoerythrins of marine unicellular cyanobacteria. II. Characterization of phycobiliproteins with unusually high phycourobilin content. J Biol Chem 266 (1991) 9528-34.

[26] S.K. Mishra, A. Shrivastav, R.R. Maurya, S.K. Patidar, S. Haldar, and S. Mishra, Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp. isolated from Gujarat coast, India. Protein Expr Purif 81 (2012) 5-10.

[27] S. Fridman, J. Flores-Uribe, S. Larom, O. Alalouf, O. Liran, I. Yacoby, F. Salama, B. Bailleul, F. Rappaport, T. Ziv, I. Sharon, F.M. Cornejo-Castillo, A. Philosof, C.L. Dupont, P. Sanchez, S.G. Acinas, F.L. Rohwer, D. Lindell, and O. Beja, A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat Microbiol 2 (2017) 1350-1357.

[28] I. Sharon, A. Alperovitch, F. Rohwer, M. Haynes, F. Glaser, N. Atamna-Ismaeel, R.Y. Pinter, F. Partensky, E.V. Koonin, Y.I. Wolf, N. Nelson, and O. Beja, Photosystem I gene cassettes are present in marine virus genomes. Nature 461 (2009) 258-262.

[29] D. Lindell, J.D. Jaffe, Z.I. Johnson, G.M. Church, and S.W. Chisholm, Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438 (2005) 86-9.

[30] A. Millard, M.R. Clokie, D.A. Shub, and N.H. Mann, Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci U S A 101 (2004) 11007-12.

[31] D. Lindell, M.B. Sullivan, Z.I. Johnson, A.C. Tolonen, F. Rohwer, and S.W. Chisholm, Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci U S A 101 (2004) 11013-8.

[32] N.H. Mann, A. Cook, A. Millard, S. Bailey, and M. Clokie, Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424 (2003) 741.

[33] R.S. Safferman, T.O. Diener, P.R. Desjardins, and M.E. Morris, Isolation and characterization of AS-1, a phycovirus infecting the blue-green algae, Anacystis nidulans and Synechococcus cedrorum. Virology 47 (1972) 105-113.

[34] K. Murata, Q. Zhang, J. Gerardo Galaz-Montoya, C. Fu, M.L. Coleman, M.S. Osburne, M.F. Schmid, M.B. Sullivan, S.W. Chisholm, and W. Chiu, Visualizing Adsorption of Cyanophage P-SSP7 onto Marine Prochlorococcus. Scientific Reports 7 (2017).

[35] A. Cuervo, M. Pulido-Cid, M. Chagoyen, R. Arranz, V.A. Gonzalez-Garcia, C. Garcia-Doval, J.R. Caston, J.M. Valpuesta, M.J. van Raaij, J. Martin-Benito, and J.L. Carrascosa, Structural characterization of the bacteriophage T7 tail machinery. J Biol Chem 288 (2013) 26290-9.

[36] M.L. Pedulla, M.E. Ford, J.M. Houtz, T. Karthikeyan, C. Wadsworth, J.A. Lewis, D. Jacobs-Sera, J. Falbo, J. Gross, N.R. Pannunzio, W. Brucker, V. Kumar, J. Kandasamy, L. Keenan, S. Bardarov, J. Kriakov, J.G. Lawrence, W.R. Jacobs, R.W. Hendrix, and G.F. Hatfull, Origins of Highly Mosaic Mycobacteriophage Genomes. Cell 113 (2003) 171-182.

[37] D. Lindell, J.D. Jaffe, M.L. Coleman, M.E. Futschik, I.M. Axmann, T. Rector, G. Kettler, M.B. Sullivan, R. Steen, W.R. Hess, G.M. Church, and S.W. Chisholm, Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449 (2007) 83-6.

[38] M.B. Sullivan, M.L. Coleman, P. Weigele, F. Rohwer, and S.W. Chisholm, Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3 (2005) e144.

[39] I.J. Molineux, No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol Microbiol 40 (2001) 1-8.

[40] B. Hu, W. Margolin, I.J. Molineux, and J. Liu, The bacteriophage t7 virion undergoes extensive structural remodeling during infection. Science 339 (2013) 576-9.

[41] J.T. Chang, M.F. Schmid, C. Haase-Pettingell, P.R. Weigele, J.A. King, and W. Chiu, Visualizing the structural changes of bacteriophage Epsilon15 and its Salmonella host during infection. J Mol Biol 402 (2010) 731-40.

[42] X. Liu, Q. Zhang, K. Murata, M.L. Baker, M.B. Sullivan, C. Fu, M.T. Dougherty, M.F. Schmid, M.S. Osburne, S.W. Chisholm, and W. Chiu, Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17 (2010) 830-6.

[43] P. Kemp, L.R. Garcia, and I.J. Molineux, Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 340 (2005) 307-17.

[44] A.C. Steven, B.L. Trus, J.V. Maizel, M. Unser, D.A.D. Parry, J.S. Wall, J.F. Hainfeld, and F.W. Studier, Molecular substructure of a viral receptor-recognition protein. Journal of Molecular Biology 200 (1988) 351-365.

[45] X. Liu, M. Shi, S. Kong, Y. Gao, and C. An, Cyanophage Pf-WMP4, a T7-like phage infecting the freshwater cyanobacterium Phormidium foveolarum: complete genome sequence and DNA translocation. Virology 366 (2007) 28-39.

[46] L.R. García, and I.J. Molineux, Transcription-independent DNA translocation of bacteriophage T7 DNA into Escherichia coli. Journal of Bacteriology 178 (1996) 6921-6929.

[47] L.R. Garcia, and I.J. Molineux, Translocation and specific cleavage of bacteriophage T7 DNA in vivo by EcoKI. Proceedings of the National Academy of Sciences 96 (1999) 12430-12435.

[48] D. Scholl, J. Kieleczawa, P. Kemp, J. Rush, C.C. Richardson, C. Merril, S. Adhya, and I.J. Molineux, Genomic Analysis of Bacteriophages SP6 and K1-5, an Estranged Subgroup of the T7 Supergroup. Journal of Molecular Biology 335 (2004) 1151-1171.

Cite This Work

To export a reference to this article please select a referencing stye below:

Reference Copied to Clipboard.
Reference Copied to Clipboard.
Reference Copied to Clipboard.
Reference Copied to Clipboard.
Reference Copied to Clipboard.
Reference Copied to Clipboard.
Reference Copied to Clipboard.

Related Services

View all

DMCA / Removal Request

If you are the original writer of this dissertation and no longer wish to have your work published on the UKDiss.com website then please: