Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase
<i>Acinetobacter pittii</i> is a species that belong to the <i>Acinetobacter calcoaceticus-baumannii</i> complex, increasingly recognized as major nosocomial bacterial pathogens, often associated with multiple drug-resistances. The capsule surrounding the bacteria represents...
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| Format: | Article |
| Language: | English |
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MDPI AG
2021-10-01
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| Series: | Antibiotics |
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| Online Access: | https://www.mdpi.com/2079-6382/10/11/1304 |
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| author | Rita Domingues Ana Barbosa Sílvio B. Santos Diana Priscila Pires Jonathan Save Grégory Resch Joana Azeredo Hugo Oliveira |
| author_facet | Rita Domingues Ana Barbosa Sílvio B. Santos Diana Priscila Pires Jonathan Save Grégory Resch Joana Azeredo Hugo Oliveira |
| author_sort | Rita Domingues |
| collection | DOAJ |
| description | <i>Acinetobacter pittii</i> is a species that belong to the <i>Acinetobacter calcoaceticus-baumannii</i> complex, increasingly recognized as major nosocomial bacterial pathogens, often associated with multiple drug-resistances. The capsule surrounding the bacteria represents a main virulence factor, helping cells avoid phage predation and host immunity. Accordingly, a better understanding of the phage infection mechanisms is required to efficiently develop phage therapy against <i>Acinetobacter</i> of different capsular types. Here, we report the isolation of the novel <i>A. pittii</i>-infecting Fri1-like phage vB_Api_3043-K38 (3043-K38) of the <i>Podoviridae</i> morphotype, from sewage samples. Its 41,580 bp linear double-stranded DNA genome harbours 53 open reading frames and 302 bp of terminal repeats. We show that all studied <i>Acinetobacter</i> Fri1-like viruses have highly similar genomes, which differentiate only at the genes coding for tailspike, likely to adapt to different host receptors. The isolated phage 3043-K38 specifically recognizes an untapped <i>Acinetobacter</i> K38 capsule type via a novel tailspike with K38 depolymerase activity. The recombinant K38 depolymerase region of the tailspike (center-end region) forms a thermostable trimer, and quickly degrades capsules. When the K38 depolymerase is applied to the cells, it makes them resistant to phage predation. Interestingly, while K38 depolymerase treatments do not synergize with antibiotics, it makes bacterial cells highly susceptible to the host serum complement. In summary, we characterized a novel phage-encoded K38 depolymerase, which not only advances our understanding of phage-host interactions, but could also be further explored as a new antibacterial agent against drug-resistant <i>Acinetobacter</i>. |
| first_indexed | 2024-03-10T05:46:08Z |
| format | Article |
| id | doaj.art-660a2fa98f0240419682b0d047a3eb1e |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-10T05:46:08Z |
| publishDate | 2021-10-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-660a2fa98f0240419682b0d047a3eb1e2023-11-22T22:09:38ZengMDPI AGAntibiotics2079-63822021-10-011011130410.3390/antibiotics10111304Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule DepolymeraseRita Domingues0Ana Barbosa1Sílvio B. Santos2Diana Priscila Pires3Jonathan Save4Grégory Resch5Joana Azeredo6Hugo Oliveira7Centre of Biological Engineering, University of Minho, 4710-057 Braga, PortugalCentre of Biological Engineering, University of Minho, 4710-057 Braga, PortugalCentre of Biological Engineering, University of Minho, 4710-057 Braga, PortugalCentre of Biological Engineering, University of Minho, 4710-057 Braga, PortugalDepartment of Intensive Care Medicine, Inselspital, Bern University Hospital, University of Bern, CH-3010 Bern, SwitzerlandCentre for Research and Innovation in Clinical Pharmaceutical Sciences, Lausanne University Hospital, CH-1011 Lausanne, SwitzerlandCentre of Biological Engineering, University of Minho, 4710-057 Braga, PortugalCentre of Biological Engineering, University of Minho, 4710-057 Braga, Portugal<i>Acinetobacter pittii</i> is a species that belong to the <i>Acinetobacter calcoaceticus-baumannii</i> complex, increasingly recognized as major nosocomial bacterial pathogens, often associated with multiple drug-resistances. The capsule surrounding the bacteria represents a main virulence factor, helping cells avoid phage predation and host immunity. Accordingly, a better understanding of the phage infection mechanisms is required to efficiently develop phage therapy against <i>Acinetobacter</i> of different capsular types. Here, we report the isolation of the novel <i>A. pittii</i>-infecting Fri1-like phage vB_Api_3043-K38 (3043-K38) of the <i>Podoviridae</i> morphotype, from sewage samples. Its 41,580 bp linear double-stranded DNA genome harbours 53 open reading frames and 302 bp of terminal repeats. We show that all studied <i>Acinetobacter</i> Fri1-like viruses have highly similar genomes, which differentiate only at the genes coding for tailspike, likely to adapt to different host receptors. The isolated phage 3043-K38 specifically recognizes an untapped <i>Acinetobacter</i> K38 capsule type via a novel tailspike with K38 depolymerase activity. The recombinant K38 depolymerase region of the tailspike (center-end region) forms a thermostable trimer, and quickly degrades capsules. When the K38 depolymerase is applied to the cells, it makes them resistant to phage predation. Interestingly, while K38 depolymerase treatments do not synergize with antibiotics, it makes bacterial cells highly susceptible to the host serum complement. In summary, we characterized a novel phage-encoded K38 depolymerase, which not only advances our understanding of phage-host interactions, but could also be further explored as a new antibacterial agent against drug-resistant <i>Acinetobacter</i>.https://www.mdpi.com/2079-6382/10/11/1304<i>Acinetobacter baumannii</i>bacteriophagetailspikedepolymeraseanti-virulencecapsule |
| spellingShingle | Rita Domingues Ana Barbosa Sílvio B. Santos Diana Priscila Pires Jonathan Save Grégory Resch Joana Azeredo Hugo Oliveira Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase Antibiotics <i>Acinetobacter baumannii</i> bacteriophage tailspike depolymerase anti-virulence capsule |
| title | Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase |
| title_full | Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase |
| title_fullStr | Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase |
| title_full_unstemmed | Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase |
| title_short | Unpuzzling Friunavirus-Host Interactions One Piece at a Time: Phage Recognizes <i>Acinetobacter pittii</i> via a New K38 Capsule Depolymerase |
| title_sort | unpuzzling friunavirus host interactions one piece at a time phage recognizes i acinetobacter pittii i via a new k38 capsule depolymerase |
| topic | <i>Acinetobacter baumannii</i> bacteriophage tailspike depolymerase anti-virulence capsule |
| url | https://www.mdpi.com/2079-6382/10/11/1304 |
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