Abstract
Five newly isolated mycobacteriophages -Angelica, CrimD, Adephagia, Anaya, and Pixie - have similar genomic architectures to mycobacteriophage TM4, a previously characterized phage that is widely used in mycobacterial genetics. The nucleotide sequence similarities warrant grouping these into Cluster K, with subdivision into three subclusters: K1, K2, and K3. Although the overall genome architectures of these phages are similar, TM4 appears to have lost at least two segments of its genome, a central region containing the integration apparatus, and a segment at the right end. This suggests that TM4 is a recent derivative of a temperate parent, resolving a long-standing conundrum about its biology, in that it was reportedly recovered from a lysogenic strain of Mycobacterium avium, but it is not capable of forming lysogens in any mycobacterial host. Like TM4, all of the Cluster K phages infect both fast- and slow-growing mycobacteria, and all of them - with the exception of TM4 - form stable lysogens in both Mycobacterium smegmatis and Mycobacterium tuberculosis; immunity assays show that all five of these phages share the same immune specificity. TM4 infects these lysogens suggesting that it was either derived from a heteroimmune temperate parent or that it has acquired a virulent phenotype. We have also characterized a widely-used conditionally replicating derivative of TM4 and identified mutations conferring the temperature-sensitive phenotype. All of the Cluster K phages contain a series of well conserved 13 bp repeats associated with the translation initiation sites of a subset of the genes; approximately one half of these contain an additional sequence feature composed of imperfectly conserved 17 bp inverted repeats separated by a variable spacer. The K1 phages integrate into the host tmRNA and the Cluster K phages represent potential new tools for the genetics of M. tuberculosis and related species.
| Original language | English (US) |
|---|---|
| Article number | e26750 |
| Journal | PLoS One |
| Volume | 6 |
| Issue number | 10 |
| DOIs | |
| State | Published - 2011 |
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ASJC Scopus subject areas
- Agricultural and Biological Sciences(all)
- Biochemistry, Genetics and Molecular Biology(all)
- Medicine(all)
Cite this
Cluster k mycobacteriophages : Insights into the evolutionary origins of mycobacteriophage tm4. / Pope, Welkin H.; Ferreira, Christina M.; Jacobs-Sera, Deborah; Benjamin, Robert C.; Davis, Ariangela J.; DeJong, Randall J.; Elgin, Sarah C R; Guilfoile, Forrest R.; Forsyth, Mark H.; Harris, Alexander D.; Harvey, Samuel E.; Hughes, Lee E.; Hynes, Peter M.; Jackson, Arrykka S.; Jalal, Marilyn D.; MacMurray, Elizabeth A.; Manley, Coreen M.; McDonough, Molly J.; Mosier, Jordan L.; Osterbann, Larissa J.; Rabinowitz, Hannah S.; Rhyan, Corwin N.; Russell, Daniel A.; Saha, Margaret S.; Shaffer, Christopher D.; Simon, Stephanie E.; Sims, Erika F.; Tovar, Isabel G.; Weisser, Emilie G.; Wertz, John T.; Weston-Hafer, Kathleen A.; Williamson, Kurt E.; Zhang, Bo; Cresawn, Steven G.; Jain, Paras; Piuri, Mariana; Jacobs, William R.; Hendrix, Roger W.; Hatfull, Graham F.
In: PLoS One, Vol. 6, No. 10, e26750, 2011.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Cluster k mycobacteriophages
T2 - Insights into the evolutionary origins of mycobacteriophage tm4
AU - Pope, Welkin H.
AU - Ferreira, Christina M.
AU - Jacobs-Sera, Deborah
AU - Benjamin, Robert C.
AU - Davis, Ariangela J.
AU - DeJong, Randall J.
AU - Elgin, Sarah C R
AU - Guilfoile, Forrest R.
AU - Forsyth, Mark H.
AU - Harris, Alexander D.
AU - Harvey, Samuel E.
AU - Hughes, Lee E.
AU - Hynes, Peter M.
AU - Jackson, Arrykka S.
AU - Jalal, Marilyn D.
AU - MacMurray, Elizabeth A.
AU - Manley, Coreen M.
AU - McDonough, Molly J.
AU - Mosier, Jordan L.
AU - Osterbann, Larissa J.
AU - Rabinowitz, Hannah S.
AU - Rhyan, Corwin N.
AU - Russell, Daniel A.
AU - Saha, Margaret S.
AU - Shaffer, Christopher D.
AU - Simon, Stephanie E.
AU - Sims, Erika F.
AU - Tovar, Isabel G.
AU - Weisser, Emilie G.
AU - Wertz, John T.
AU - Weston-Hafer, Kathleen A.
AU - Williamson, Kurt E.
AU - Zhang, Bo
AU - Cresawn, Steven G.
AU - Jain, Paras
AU - Piuri, Mariana
AU - Jacobs, William R.
AU - Hendrix, Roger W.
AU - Hatfull, Graham F.
PY - 2011
Y1 - 2011
N2 - Five newly isolated mycobacteriophages -Angelica, CrimD, Adephagia, Anaya, and Pixie - have similar genomic architectures to mycobacteriophage TM4, a previously characterized phage that is widely used in mycobacterial genetics. The nucleotide sequence similarities warrant grouping these into Cluster K, with subdivision into three subclusters: K1, K2, and K3. Although the overall genome architectures of these phages are similar, TM4 appears to have lost at least two segments of its genome, a central region containing the integration apparatus, and a segment at the right end. This suggests that TM4 is a recent derivative of a temperate parent, resolving a long-standing conundrum about its biology, in that it was reportedly recovered from a lysogenic strain of Mycobacterium avium, but it is not capable of forming lysogens in any mycobacterial host. Like TM4, all of the Cluster K phages infect both fast- and slow-growing mycobacteria, and all of them - with the exception of TM4 - form stable lysogens in both Mycobacterium smegmatis and Mycobacterium tuberculosis; immunity assays show that all five of these phages share the same immune specificity. TM4 infects these lysogens suggesting that it was either derived from a heteroimmune temperate parent or that it has acquired a virulent phenotype. We have also characterized a widely-used conditionally replicating derivative of TM4 and identified mutations conferring the temperature-sensitive phenotype. All of the Cluster K phages contain a series of well conserved 13 bp repeats associated with the translation initiation sites of a subset of the genes; approximately one half of these contain an additional sequence feature composed of imperfectly conserved 17 bp inverted repeats separated by a variable spacer. The K1 phages integrate into the host tmRNA and the Cluster K phages represent potential new tools for the genetics of M. tuberculosis and related species.
AB - Five newly isolated mycobacteriophages -Angelica, CrimD, Adephagia, Anaya, and Pixie - have similar genomic architectures to mycobacteriophage TM4, a previously characterized phage that is widely used in mycobacterial genetics. The nucleotide sequence similarities warrant grouping these into Cluster K, with subdivision into three subclusters: K1, K2, and K3. Although the overall genome architectures of these phages are similar, TM4 appears to have lost at least two segments of its genome, a central region containing the integration apparatus, and a segment at the right end. This suggests that TM4 is a recent derivative of a temperate parent, resolving a long-standing conundrum about its biology, in that it was reportedly recovered from a lysogenic strain of Mycobacterium avium, but it is not capable of forming lysogens in any mycobacterial host. Like TM4, all of the Cluster K phages infect both fast- and slow-growing mycobacteria, and all of them - with the exception of TM4 - form stable lysogens in both Mycobacterium smegmatis and Mycobacterium tuberculosis; immunity assays show that all five of these phages share the same immune specificity. TM4 infects these lysogens suggesting that it was either derived from a heteroimmune temperate parent or that it has acquired a virulent phenotype. We have also characterized a widely-used conditionally replicating derivative of TM4 and identified mutations conferring the temperature-sensitive phenotype. All of the Cluster K phages contain a series of well conserved 13 bp repeats associated with the translation initiation sites of a subset of the genes; approximately one half of these contain an additional sequence feature composed of imperfectly conserved 17 bp inverted repeats separated by a variable spacer. The K1 phages integrate into the host tmRNA and the Cluster K phages represent potential new tools for the genetics of M. tuberculosis and related species.
UR - http://www.scopus.com/inward/record.url?scp=80055027771&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=80055027771&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0026750
DO - 10.1371/journal.pone.0026750
M3 - Article
C2 - 22053209
AN - SCOPUS:80055027771
VL - 6
JO - PLoS One
JF - PLoS One
SN - 1932-6203
IS - 10
M1 - e26750
ER -