Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance

<i>Lactococcus lactis </i>is the most widely exploited microorganism in global dairy fermentations. Lactococcal strains are described as typically harboring a number of prophages in their chromosomes. The presence of such prophages may provide both advantages and disadvantages to the car...

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Main Authors: Sofia Ruiz Cruz, Elvina Parlindungan, Andrea Erazo Garzon, Mona Alqarni, Gabriele A. Lugli, Marco Ventura, Douwe van Sinderen, Jennifer Mahony
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/11/1685
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spelling doaj-9d8ec872a02849f1ba279a499fe89f922020-11-25T03:10:08ZengMDPI AGMicroorganisms2076-26072020-10-0181685168510.3390/microorganisms8111685Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage ResistanceSofia Ruiz Cruz0Elvina Parlindungan1Andrea Erazo Garzon2Mona Alqarni3Gabriele A. Lugli4Marco Ventura5Douwe van Sinderen6Jennifer Mahony7School of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, IrelandSchool of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, IrelandSchool of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, IrelandSchool of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, IrelandLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, 43121 Parma, ItalyLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, 43121 Parma, ItalySchool of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, IrelandSchool of Microbiology & APC Microbiome Ireland, University College Cork, Western Road, Cork T12 YT20, Ireland<i>Lactococcus lactis </i>is the most widely exploited microorganism in global dairy fermentations. Lactococcal strains are described as typically harboring a number of prophages in their chromosomes. The presence of such prophages may provide both advantages and disadvantages to the carrying host. Here, we describe the deliberate generation of three distinct lysogens of the model lactococcal strain 3107 and the impact of additional prophage carriage on phage-resistance and anti-microbial susceptibility. Lysogen-specific responses were observed, highlighting the unique relationship and impact of each lysogenic phage on its host. Both homologous and heterologous phage-resistance profiles were observed, highlighting the presence of possible prophage-encoded phage-resistance factors. Superinfection exclusion was among the most notable causes of heterologous phage-resistance profiles with resistance observed against members of the <i>Skunavirus</i>, P335, P087, and 949 lactococcal phage groups. Through these analyses, it is now possible to identify phages that may pursue similar DNA injection pathways. The generated lysogenic strains exhibited increased sensitivity to the antimicrobial compounds, nisin and lysozyme, relative to the parent strain, although it is noteworthy that the degree of sensitivity was specific to the individual (pro)phages. Overall, the findings highlight the unique impact of each prophage on a given strain and the requirement for strain-level analysis when considering the implications of lysogeny.https://www.mdpi.com/2076-2607/8/11/1685bacteriophage<i>Lactococcus lactis</i>prophagephage-resistanceabortive infection
collection DOAJ
language English
format Article
sources DOAJ
author Sofia Ruiz Cruz
Elvina Parlindungan
Andrea Erazo Garzon
Mona Alqarni
Gabriele A. Lugli
Marco Ventura
Douwe van Sinderen
Jennifer Mahony
spellingShingle Sofia Ruiz Cruz
Elvina Parlindungan
Andrea Erazo Garzon
Mona Alqarni
Gabriele A. Lugli
Marco Ventura
Douwe van Sinderen
Jennifer Mahony
Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
Microorganisms
bacteriophage
<i>Lactococcus lactis</i>
prophage
phage-resistance
abortive infection
author_facet Sofia Ruiz Cruz
Elvina Parlindungan
Andrea Erazo Garzon
Mona Alqarni
Gabriele A. Lugli
Marco Ventura
Douwe van Sinderen
Jennifer Mahony
author_sort Sofia Ruiz Cruz
title Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
title_short Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
title_full Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
title_fullStr Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
title_full_unstemmed Lysogenization of a Lactococcal Host with Three Distinct Temperate Phages Provides Homologous and Heterologous Phage Resistance
title_sort lysogenization of a lactococcal host with three distinct temperate phages provides homologous and heterologous phage resistance
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2020-10-01
description <i>Lactococcus lactis </i>is the most widely exploited microorganism in global dairy fermentations. Lactococcal strains are described as typically harboring a number of prophages in their chromosomes. The presence of such prophages may provide both advantages and disadvantages to the carrying host. Here, we describe the deliberate generation of three distinct lysogens of the model lactococcal strain 3107 and the impact of additional prophage carriage on phage-resistance and anti-microbial susceptibility. Lysogen-specific responses were observed, highlighting the unique relationship and impact of each lysogenic phage on its host. Both homologous and heterologous phage-resistance profiles were observed, highlighting the presence of possible prophage-encoded phage-resistance factors. Superinfection exclusion was among the most notable causes of heterologous phage-resistance profiles with resistance observed against members of the <i>Skunavirus</i>, P335, P087, and 949 lactococcal phage groups. Through these analyses, it is now possible to identify phages that may pursue similar DNA injection pathways. The generated lysogenic strains exhibited increased sensitivity to the antimicrobial compounds, nisin and lysozyme, relative to the parent strain, although it is noteworthy that the degree of sensitivity was specific to the individual (pro)phages. Overall, the findings highlight the unique impact of each prophage on a given strain and the requirement for strain-level analysis when considering the implications of lysogeny.
topic bacteriophage
<i>Lactococcus lactis</i>
prophage
phage-resistance
abortive infection
url https://www.mdpi.com/2076-2607/8/11/1685
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