Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus
ABSTRACT In a survey of a waterway on Wurundjeri land, two sub-populations of the bacteriophage Merri-merri-uth nyilam marra-natj (phage MMNM) were isolated on a permissive host, Klebsiella B5055 of capsule-type K2, but were distinguished by minor phenotypic differences. The variant phage MMNM(Ala13...
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American Society for Microbiology
2024-12-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02564-24 |
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| author | Tze Y. Thung Alex Hall Afif P. Jati Murray E. White Rebecca S. Bamert Kher Shing Tan Cara Press George Taiaroa Francesca L. Short Rhys A. Dunstan Trevor Lithgow |
| author_facet | Tze Y. Thung Alex Hall Afif P. Jati Murray E. White Rebecca S. Bamert Kher Shing Tan Cara Press George Taiaroa Francesca L. Short Rhys A. Dunstan Trevor Lithgow |
| author_sort | Tze Y. Thung |
| collection | DOAJ |
| description | ABSTRACT In a survey of a waterway on Wurundjeri land, two sub-populations of the bacteriophage Merri-merri-uth nyilam marra-natj (phage MMNM) were isolated on a permissive host, Klebsiella B5055 of capsule-type K2, but were distinguished by minor phenotypic differences. The variant phage MMNM(Ala134) showed an inhibited activity against Klebsiella AJ174-2, and this was used as a basis to select for further variation through experimental evolution. Over the course of an evolution experiment, 20 phages that evolved distinct phenotypes in terms of the morphologies of plaques formed when they infected host Klebsiella were subject to whole-genome sequencing. The evolved phages had mutations in a small set of proteins that contribute to the baseplate portion of the phage virion. Phages MMNM and MMNM(Ala134) are minimalist phages, with baseplates formed from only five predicted subunits, akin to other minimalist phages Pam3 and XM1. The homology between all three minimalist phages provided a structural framework to interpret the two classes of mutations derived through evolution in the presence of the semi-permissive host: those that affect the interfacial surfaces between baseplate subunits, and those in a base-plate associated tail-fiber. This study evidences that multiple small mutations can be fixed into a sub-population of phage to provide a basis for phenotypic variation that we suggest could ultimately provide for a shift of virus properties, as an alternative evolutionary scenario to the major genetic events that result in more well-studied evolutionary mechanism of phage mosaicism.IMPORTANCEBacteriophages (phages) are viruses that prey on bacteria. This study sampled natural phage populations to test the hypothesis that untapped genetic variation within a population can be the basis for the selection of phages to diversify their host-range. Sampling of a freshwater site revealed two populations of the phage Merri-merri-uth nyilam marra-natj (phage MMNM), differing by a variant residue (Val134Ala) in the baseplate protein MMNM_26. This sequence variation modulated bacterial killing in plaques, and further evolution of the phages on a semi-permissive bacterial host led to a new generation of phages with more diverse phenotypes in killing the bacterium Klebsiella pneumoniae. |
| format | Article |
| id | doaj-art-f74f0e64a3ee4855a1bdd33a09d86f81 |
| institution | Kabale University |
| issn | 2150-7511 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | American Society for Microbiology |
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| series | mBio |
| spelling | doaj-art-f74f0e64a3ee4855a1bdd33a09d86f812024-12-11T14:02:30ZengAmerican Society for MicrobiologymBio2150-75112024-12-01151210.1128/mbio.02564-24Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virusTze Y. Thung0Alex Hall1Afif P. Jati2Murray E. White3Rebecca S. Bamert4Kher Shing Tan5Cara Press6George Taiaroa7Francesca L. Short8Rhys A. Dunstan9Trevor Lithgow10Center to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaDepartment of Microbiology and Immunology, The Peter Doherty Institute, The University of Melbourne, Parkville, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaCenter to Impact AMR, Monash University, Clayton, AustraliaABSTRACT In a survey of a waterway on Wurundjeri land, two sub-populations of the bacteriophage Merri-merri-uth nyilam marra-natj (phage MMNM) were isolated on a permissive host, Klebsiella B5055 of capsule-type K2, but were distinguished by minor phenotypic differences. The variant phage MMNM(Ala134) showed an inhibited activity against Klebsiella AJ174-2, and this was used as a basis to select for further variation through experimental evolution. Over the course of an evolution experiment, 20 phages that evolved distinct phenotypes in terms of the morphologies of plaques formed when they infected host Klebsiella were subject to whole-genome sequencing. The evolved phages had mutations in a small set of proteins that contribute to the baseplate portion of the phage virion. Phages MMNM and MMNM(Ala134) are minimalist phages, with baseplates formed from only five predicted subunits, akin to other minimalist phages Pam3 and XM1. The homology between all three minimalist phages provided a structural framework to interpret the two classes of mutations derived through evolution in the presence of the semi-permissive host: those that affect the interfacial surfaces between baseplate subunits, and those in a base-plate associated tail-fiber. This study evidences that multiple small mutations can be fixed into a sub-population of phage to provide a basis for phenotypic variation that we suggest could ultimately provide for a shift of virus properties, as an alternative evolutionary scenario to the major genetic events that result in more well-studied evolutionary mechanism of phage mosaicism.IMPORTANCEBacteriophages (phages) are viruses that prey on bacteria. This study sampled natural phage populations to test the hypothesis that untapped genetic variation within a population can be the basis for the selection of phages to diversify their host-range. Sampling of a freshwater site revealed two populations of the phage Merri-merri-uth nyilam marra-natj (phage MMNM), differing by a variant residue (Val134Ala) in the baseplate protein MMNM_26. This sequence variation modulated bacterial killing in plaques, and further evolution of the phages on a semi-permissive bacterial host led to a new generation of phages with more diverse phenotypes in killing the bacterium Klebsiella pneumoniae.https://journals.asm.org/doi/10.1128/mbio.02564-24Klebsiellaphage receptordepolymerasephage baseplatecommunity moduleethical bioprospecting |
| spellingShingle | Tze Y. Thung Alex Hall Afif P. Jati Murray E. White Rebecca S. Bamert Kher Shing Tan Cara Press George Taiaroa Francesca L. Short Rhys A. Dunstan Trevor Lithgow Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus mBio Klebsiella phage receptor depolymerase phage baseplate community module ethical bioprospecting |
| title | Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus |
| title_full | Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus |
| title_fullStr | Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus |
| title_full_unstemmed | Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus |
| title_short | Genetic variation in individuals from a population of the minimalist bacteriophage Merri-merri-uth nyilam marra-natj driving evolution of the virus |
| title_sort | genetic variation in individuals from a population of the minimalist bacteriophage merri merri uth nyilam marra natj driving evolution of the virus |
| topic | Klebsiella phage receptor depolymerase phage baseplate community module ethical bioprospecting |
| url | https://journals.asm.org/doi/10.1128/mbio.02564-24 |
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