A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496

Streptococcus thermophilus is considered one of the most important species for the dairy industry. Due to their diffusion in dairy environments, bacteriophages can represent a threat to this widely used bacterial species. Despite the presence of a CRISPR-Cas system in the S. thermophilus genome, som...

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Main Authors: Vinícius da Silva Duarte, Sabrina Giaretta, Stefano Campanaro, Laura Treu, Andrea Armani, Armin Tarrah, Sérgio Oliveira de Paula, Alessio Giacomini, Viviana Corich
Format: Article
Language:English
Published: MDPI AG 2018-12-01
Series:Viruses
Subjects:
Online Access:http://www.mdpi.com/1999-4915/11/1/7
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author Vinícius da Silva Duarte
Sabrina Giaretta
Stefano Campanaro
Laura Treu
Andrea Armani
Armin Tarrah
Sérgio Oliveira de Paula
Alessio Giacomini
Viviana Corich
author_facet Vinícius da Silva Duarte
Sabrina Giaretta
Stefano Campanaro
Laura Treu
Andrea Armani
Armin Tarrah
Sérgio Oliveira de Paula
Alessio Giacomini
Viviana Corich
author_sort Vinícius da Silva Duarte
collection DOAJ
description Streptococcus thermophilus is considered one of the most important species for the dairy industry. Due to their diffusion in dairy environments, bacteriophages can represent a threat to this widely used bacterial species. Despite the presence of a CRISPR-Cas system in the S. thermophilus genome, some lysogenic strains harbor cryptic prophages that can increase the phage-host resistance defense. This characteristic was identified in the dairy strain S. thermophilus M17PTZA496, which contains two integrated prophages 51.8 and 28.3 Kb long, respectively. In the present study, defense mechanisms, such as a lipoprotein-encoding gene and Siphovirus Gp157, the last associated to the presence of a noncoding viral DNA element, were identified in the prophage M17PTZA496 genome. The ability to overexpress genes involved in these defense mechanisms under specific stressful conditions, such as phage attack, has been demonstrated. Despite the addition of increasing amounts of Mitomycin C, M17PTZA496 was found to be non-inducible. However, the transcriptional activity of the phage terminase large subunit was detected in the presence of the antagonist phage vB_SthS-VA460 and of Mitomycin C. The discovery of an additional immune mechanism, associated with bacteriophage-insensitive strains, is of utmost importance, for technological applications and industrial processes. To our knowledge, this is the first study reporting the capability of a prophage integrated into the S. thermophilus genome expressing different phage defense mechanisms. Bacteriophages are widespread entities that constantly threaten starter cultures in the dairy industry. In cheese and yogurt manufacturing, the lysis of Streptococcus thermophilus cultures by viral attacks can lead to huge economic losses. Nowadays S. thermophilus is considered a well-stablished model organism for the study of natural adaptive immunity (CRISPR-Cas) against phage and plasmids, however, the identification of novel bacteriophage-resistance mechanisms, in this species, is strongly desirable. Here, we demonstrated that the presence of a non-inducible prophage confers phage-immunity to an S. thermophilus strain, by the presence of ltp and a viral noncoding region. S. thermophilus M17PTZA496 arises as an unconventional model to study phage resistance and potentially represents an alternative starter strain for dairy productions.
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spelling doaj.art-95b40cc9218445d3ab2d94350978d6492022-12-22T00:35:15ZengMDPI AGViruses1999-49152018-12-01111710.3390/v11010007v11010007A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496Vinícius da Silva Duarte0Sabrina Giaretta1Stefano Campanaro2Laura Treu3Andrea Armani4Armin Tarrah5Sérgio Oliveira de Paula6Alessio Giacomini7Viviana Corich8Department of Microbiology, Universidade Federal de Viçosa, Av. Peter Henry Rolfs, s/n, Campus Universitário, Viçosa-MG 36570-900, BrazilDepartment of Agronomy Food Natural Resources Animals and Environment, University of Padova, 35020 Legnaro, ItalyDepartment of Biology, University of Padova, 35121 Padova, ItalyDepartment of Agronomy Food Natural Resources Animals and Environment, University of Padova, 35020 Legnaro, ItalyVenetian Institute of Molecular Medicine, 35129 Padova, ItalyDepartment of Agronomy Food Natural Resources Animals and Environment, University of Padova, 35020 Legnaro, ItalyDepartment of General Biology, Universidade Federal de Viçosa, Viçosa-MG 36570-900, BrazilDepartment of Agronomy Food Natural Resources Animals and Environment, University of Padova, 35020 Legnaro, ItalyDepartment of Agronomy Food Natural Resources Animals and Environment, University of Padova, 35020 Legnaro, ItalyStreptococcus thermophilus is considered one of the most important species for the dairy industry. Due to their diffusion in dairy environments, bacteriophages can represent a threat to this widely used bacterial species. Despite the presence of a CRISPR-Cas system in the S. thermophilus genome, some lysogenic strains harbor cryptic prophages that can increase the phage-host resistance defense. This characteristic was identified in the dairy strain S. thermophilus M17PTZA496, which contains two integrated prophages 51.8 and 28.3 Kb long, respectively. In the present study, defense mechanisms, such as a lipoprotein-encoding gene and Siphovirus Gp157, the last associated to the presence of a noncoding viral DNA element, were identified in the prophage M17PTZA496 genome. The ability to overexpress genes involved in these defense mechanisms under specific stressful conditions, such as phage attack, has been demonstrated. Despite the addition of increasing amounts of Mitomycin C, M17PTZA496 was found to be non-inducible. However, the transcriptional activity of the phage terminase large subunit was detected in the presence of the antagonist phage vB_SthS-VA460 and of Mitomycin C. The discovery of an additional immune mechanism, associated with bacteriophage-insensitive strains, is of utmost importance, for technological applications and industrial processes. To our knowledge, this is the first study reporting the capability of a prophage integrated into the S. thermophilus genome expressing different phage defense mechanisms. Bacteriophages are widespread entities that constantly threaten starter cultures in the dairy industry. In cheese and yogurt manufacturing, the lysis of Streptococcus thermophilus cultures by viral attacks can lead to huge economic losses. Nowadays S. thermophilus is considered a well-stablished model organism for the study of natural adaptive immunity (CRISPR-Cas) against phage and plasmids, however, the identification of novel bacteriophage-resistance mechanisms, in this species, is strongly desirable. Here, we demonstrated that the presence of a non-inducible prophage confers phage-immunity to an S. thermophilus strain, by the presence of ltp and a viral noncoding region. S. thermophilus M17PTZA496 arises as an unconventional model to study phage resistance and potentially represents an alternative starter strain for dairy productions.http://www.mdpi.com/1999-4915/11/1/7Streptococcus thermophiluslipoprotein (Ltp)noncoding regionbacteriophagescryptic prophage
spellingShingle Vinícius da Silva Duarte
Sabrina Giaretta
Stefano Campanaro
Laura Treu
Andrea Armani
Armin Tarrah
Sérgio Oliveira de Paula
Alessio Giacomini
Viviana Corich
A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
Viruses
Streptococcus thermophilus
lipoprotein (Ltp)
noncoding region
bacteriophages
cryptic prophage
title A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
title_full A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
title_fullStr A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
title_full_unstemmed A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
title_short A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
title_sort cryptic non inducible prophage confers phage immunity on the streptococcus thermophilus m17ptza496
topic Streptococcus thermophilus
lipoprotein (Ltp)
noncoding region
bacteriophages
cryptic prophage
url http://www.mdpi.com/1999-4915/11/1/7
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