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Unusual Helicases

Found in Erwinia phage RAYEmily Jacobs, Katrina Saam, Ryan Koch, Melissa Guereca�1Division of Biological Sciences, Section of Molecular Biology, University of California, San Diego, La Jolla, United States

Goal: To study the Erwinia phage RAY proteins gp131 and gp250 with the intent of forming a conclusion about the functions of these proteins.

  • Understanding Erwinia phage could help us understand other types of bacterial infections in related hosts, help develop phage therapy to treat Erwinia infections in plants, teach us more about jumbophage function through the study of these unknown proteins, etc.

What is RAY?

  • RAY is one of nine closely related jumbo phages that are members of the bacteriophage family Agrican357virus.
    • Primarily infects Erwinia amylovora but is known to infect a few other bacterial species as well.

What is Erwinia amylovora?

  • Erwinia amylovora causes fire blight, a bacterial infection that mainly harms ornamental plants of the Rosaceae family.

What are jumbo phage?

  • Jumbo phage are phage that have unusually large genomes.
  • Upon infection, jumbo phage create their own nucleus within the bacterial cell known as the phage nucleus, in which the phage DNA is transcribed and stored until the capsids can be filled.

What is the SWI/SNF complex?

  • Chromatin-remodeling complex consisting of 12 subunits found exclusively in eukaryotes that is responsible for shifting/removing nucleosomes to allow or restrict access to the DNA for gene expression, repair, and replication.

What is a DEAD-box helicase?

  • Family of ATP-dependant RNA and DNA helicases found in both prokaryotes and eukaryotes that performs a wide variety of functions.
  • The SNF helicase family is a family of DEAD-like helicases belonging to the superfamily SF2 that includes chromatin remodeling factors and recombination proteins. This is the same family to which the SWI/SNF complex belongs.

Rationale/Background

Hypothesis

Localization

  • Used Benchling to design a plasmid containing the sequence for our protein.
  • Transformed the plasmid into Erwinia and added arabinose to the cells.
  • Infected the cells with RAY and used fluorescence microscopy to image them.

PSI-BLAST and Conserved Domain Process

  • Identified homologs through 5 iterations of PSI-BLAST using the amino acid sequence for each protein, deselecting all hits with an e-value below the threshold before each new iteration.
  • Ran each protein’s amino acid sequence through the NCBI Conserved Domain Database to identify any conserved domains.

iTOL Tree Process

  • Used VIPTree to analyse the relationship between RAY and other related phage.
  • Uploaded VIPTree output into iTOL and annotated branches to identify jumbo phage and homologs.

Sequence Alignments Process

  • Aligned gp131/gp250 with its homologs using Clustal-Omega and visualized results using ESPript.

Protein Homologue Tree Process

  • Used PhyML to bootstrap a tree relating gp131/gp250 to their homologs 100 times.
  • Finalized tree in iTOL and used as a comparison with the relationships found in the full genome phylogenetic tree.

Experimental Approach

Figure 5. Sequence alignment comparing the amino acid sequences of gp131(top) and gp250 homologs (bottom). Blue boxes indicate regions in which there is a large amount of conservation between the sequences. Amino acids that are identical or similar to the column consensus are colored in red, and if the entire column shares the exact same amino acid, the sequences are highlighted in red. The light yellow highlighted regions are the highest significance conserved domains of gp250: SSL 2 which functions as a general RNA or DNA helicase and SF2_C, a structure of C-terminal helicase of superfamily 2 DEAD/H-box helicases. The bright yellow highlighted region is the DEXDc conserved region of gp131 which indicates a DEAD-like helicase that includes chromatin remodeling factors and recombination proteins. The green highlighted region is the HELICc conserved domain of gp131 which indicates a function of a helicase with a c-terminal domain. The protein homolog sequences that appear to exhibit the most similarity to both gp131 and gp250 are helicases and hypothetical proteins from Salmonella phage vB SaIM SA002 and Proteus phage 10.

Inferences and Conclusions

PSI-BLAST Search for Protein Homologs (gp131): The two proteins with the most similarity to gp131 are the putative DEAD-like helicase from Erwinia phage DesertFox and the DEAD-like helicase from Erwinia phage Ea35-70, each with a 99% identity to gp131. The proteins with highest identities to gp131 after these two are the putative DEAD-like helicase from Salmonella phage vB_SalM_SA002 and a hypothetical protein from Proteus phage 10.

iTOL Phage Phylogenetic Tree (gp131): gp131 is found primarily in jumbo phages, indicating that it is probably more useful to jumbophage than to regular phage. This makes sense given that gp131 likely has something to do with packaging and organizing DNA, a function that is probably more important in a phage with more DNA.

PSI-BLAST Search for Protein Homologues (gp250): Out of the 36 hits, the proteins most similar to gp250 are Erwinia phage Desertfox and Erwinia phage Ea35-70 which each contain a 99.61% identity, which are both part of the Superfamily 2 DNA/RNA helicase. The phage most similar to gp250 outside the Erwinia family, is Salmonella phage SA002, with a identity of 69.11%, which according to the NCBI database states this phage has the conserved structure of a replicative helicase.

iTOL Phage Phylogenetic Tree (gp250): The phage tree demonstrates that gp250 is highly conserved across most jumbo phage. Erwinia phage Desertfox showed to be most common to gp250. Outside of the Erwinia family the phage most common to gp250 is Salmonella phage SA002. This demonstrates that gp250 is an important protein for jumbo phage because as these phage evolved they predominantly preserved homologs of gp250, likely to unpack the >200 kpb of viral genome.

CONCLUSIONS: From these results, we can conclude that gp131 is a DEAD-like SWI/SNF related helicase that functions in genome packaging and organization. Likewise, gp250 functions as a helicase in the process of chromatin remodeling, potentially as a RAD2/SF2 helicase.

Results, cont.

  • Future research on this topic might involve looking into the mechanism behind these proteins. Do they involve the use of a histone-like protein that exists in phage, or do they use some other mechanism to organize and package DNA?
  • gp250’s inhibition of phage infection remains unexplained by our results. Future research could also pursue a more in-depth look at the protein’s behavior/evolutionary history to discern why how the observed localization patterns came to be.
  • We might also want to research homologs that exist in closely related phage to gain insight into the how these proteins work, their roles in the infection process, and for what reasons they are necessary to certain phage.

Figure 3C. Erwinia cell infected with RAY phage, tagged for gp131 localization. The first row shows images from the cells containing 0.5% arabinose 80 minutes post infection (mpi), and the second row shows images from cells containing no arabinose 80 mpi. gp131 (stained in green) localizes outside of the phage nucleus, which is defined by the presence of the DNA (stained in blue), and in the cytoplasm. This indicates that gp131 localizes exclusively within the cytoplasm during the viral replication process.

Figure 3A. Uninfected Erwinia cells with fluorescence. gp131’s cell ( left) exhibits overlap between the blue stain, a fluorescence protein called DAPI that stains DNA, and gp131’s green stain, indicating gp131’s presence throughout the entire cell pre-infection. gp250’s cell ( right) shows no overlap between the two.

Figure 3B. Erwinia cell infected with RAY phage, tagged for gp250 localization. The first row shows images from the cells containing 0.5% arabinose 70 minutes post infection (mpi), and the second row shows images from cells containing 0.1% arabinose 90 mpi. gp250 (stained in green) localizes inside of the phage nucleus, which is defined by the presence of the DNA (stained in blue). This indicates that gp250 localizes exclusively within the nucleus during the viral replication process.

We would like to thank Professors Rachel Dutton and Joseph Pogliano, Amy Prichard, and Tara Spencer for their assistance and guidance throughout the research process. We would also like to thank our BIMM 170 classmates for providing a supportive environment where we could complete our research, and a final thank you to Julianne H. Grose from Brigham Young University for providing us with the phage.

Future Directions

  1. Byrd, A., & Raney, K. (2012, June 1). Superfamily 2 HELICASES. Retrieved May 11, 2021, from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3775597/
  2. Liu, X., Li, M., Xia, X., Li, X., & Chen, Z. (2017, April 19). Mechanism of chromatin remodeling revealed by the snf2-nucleosome structure. Retrieved May 11, 2021, from https://www.nature.com/articles/nature22036?foxtrotcallback=true
  3. Joliot, V., Ait-Mohamed, O., Battisti, V., Pontis, J., Philipot, O., Robin, P., Ito, H., & Ait-Si-Ali, S. (2014, October 1). The SWI/SNF subunit/tumor suppressor BAF47/INI1 is essential in cell cycle arrest upon skeletal muscle terminal differentiation. Retrieved May 11, 2021, from http://europepmc.org/articles/PMC4182762
  4. Serrano, M., Gutierrez, C., Freire, R., Bravo, A., Salas, M., & Hermosa, J. (n.d.). Phage Phi 29 protein P6: A viral histone-like protein. Retrieved May 11, 2021, from https://pubmed.ncbi.nlm.nih.gov/7748942/
  5. Cdd conserved protein domain family: Sf2_c_snf. (n.d.). Retrieved May 11, 2021, from https://www.ncbi.nlm.nih.gov/Structure/cdd/cddsrv.cgi?ascbin=8&maxaln=10&seltype=2&uid=cd18793

Bibliography

Acknowledgements

We believe that gp131 and gp250 are analogous to the SWI/SNF complex found in eukaryotes.

Figure 4. Phylogenetic tree showing the distribution of RAY_gp131 and RAY_gp250 homologs. A filled in square represents high confidence alignments and an empty square represents low confidence alignments. Our results show that both gp131 and gp250 homologs are highly conserved among jumbo phage, especially gp250, which suggests that most jumbo phages require these helicases for infection.

What is the conservation of gp131 and gp250 across relatives of Erwinia phage RAY?

How closely aligned are the sequences of gp131 and gp250 with those of related proteins?

Where do gp250 and gp131 localize in the cell before and during infection?

Figure 2. Results from PHYRE2 analysis of gp131 (top) and gp250 (bottom). Both gp131 and gp250 were tagged as transcription regulatory proteins within the SWI/SNF nucleosome complex, suggesting similar functions within RAY.

What is the putative function of gp131/gp250?

Results

Figure 1. Jumbo phage nucleus. This diagram depicts the life cycle of a jumbo phage, including the formation of the phage nucleus (teal circle). The orange filaments are Phuz-like filaments the move the phage nucleus to the center of the cell and keep it centered. The blue bits in the center of the phage nucleus are the phage DNA, and the hexagons on the outside of the phage nucleus in the forth image are the phage capsids being filled with DNA.