Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation
<i>Listeria monocytogenes</i> is a Gram-positive pathogen responsible for the severe foodborne disease listeriosis. A chromosomal hotspot between <i>lmo0301</i> and <i>lmo0305</i> has been noted to harbor diverse restriction modification (RM) systems. Here, we ana...
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MDPI AG
2023-03-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/3/699 |
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| author | Phillip Brown Sangmi Lee Driss Elhanafi Wilhelm Tham Marie-Louise Danielsson-Tham Gloria Lopez-Valladares Yi Chen Mirena Ivanova Pimlapas Leekitcharoenphon Sophia Kathariou |
| author_facet | Phillip Brown Sangmi Lee Driss Elhanafi Wilhelm Tham Marie-Louise Danielsson-Tham Gloria Lopez-Valladares Yi Chen Mirena Ivanova Pimlapas Leekitcharoenphon Sophia Kathariou |
| author_sort | Phillip Brown |
| collection | DOAJ |
| description | <i>Listeria monocytogenes</i> is a Gram-positive pathogen responsible for the severe foodborne disease listeriosis. A chromosomal hotspot between <i>lmo0301</i> and <i>lmo0305</i> has been noted to harbor diverse restriction modification (RM) systems. Here, we analyzed 872 <i>L. monocytogenes</i> genomes to better understand the prevalence and types of RM systems in this region, designated the immigration control region (ICR). Type I, II, III and IV RM systems were found in 86.1% of strains inside the ICR and in 22.5% of strains flanking the ICR. ICR content was completely conserved within the same multilocus sequence typing-based sequence type (ST), but the same RM system could be identified in diverse STs. The intra-ST conservation of ICR content suggests that this region may drive the emergence of new STs and promote clone stability. Sau3AI-like, LmoJ2 and LmoJ3 type II RM systems as well as type I EcoKI-like, and type IV AspBHI-like and <i>mcrB</i>-like systems accounted for all RM systems in the ICR. A Sau3AI-like type II RM system with specificity for GATC was harbored in the ICR of many STs, including all strains of the ancient, ubiquitous ST1. The extreme paucity of GATC recognition sites in lytic phages may reflect ancient adaptation of these phages to preempt resistance associated with the widely distributed Sau3AI-like systems. These findings indicate that the ICR has a high propensity for RM systems which are intraclonaly conserved and may impact bacteriophage susceptibility as well as ST emergence and stability. |
| first_indexed | 2024-03-09T10:59:09Z |
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| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T10:59:09Z |
| publishDate | 2023-03-01 |
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| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-5c5f02192873498885d97826d39b8b082023-12-01T01:23:07ZengMDPI AGMicroorganisms2076-26072023-03-0111369910.3390/microorganisms11030699Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type ConservationPhillip Brown0Sangmi Lee1Driss Elhanafi2Wilhelm Tham3Marie-Louise Danielsson-Tham4Gloria Lopez-Valladares5Yi Chen6Mirena Ivanova7Pimlapas Leekitcharoenphon8Sophia Kathariou9Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USADepartment of Food and Nutrition, Chungbuk National University, Chengju 28644, Chungbuk, Republic of KoreaBiomanufacturing Training and Education Center, North Carolina State University, Raleigh, NC 27695, USASchool of Hospitality, Culinary Arts and Meal Science, Örebro University, 702 81 Örebro, SwedenSchool of Hospitality, Culinary Arts and Meal Science, Örebro University, 702 81 Örebro, SwedenSchool of Hospitality, Culinary Arts and Meal Science, Örebro University, 702 81 Örebro, SwedenDivision of Microbiology, Center for Food Safety and Applied Nutrition, Food and Drug Administration, College Park, MD 20740, USAResearch Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, 2800 Lyngby, DenmarkResearch Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, 2800 Lyngby, DenmarkDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA<i>Listeria monocytogenes</i> is a Gram-positive pathogen responsible for the severe foodborne disease listeriosis. A chromosomal hotspot between <i>lmo0301</i> and <i>lmo0305</i> has been noted to harbor diverse restriction modification (RM) systems. Here, we analyzed 872 <i>L. monocytogenes</i> genomes to better understand the prevalence and types of RM systems in this region, designated the immigration control region (ICR). Type I, II, III and IV RM systems were found in 86.1% of strains inside the ICR and in 22.5% of strains flanking the ICR. ICR content was completely conserved within the same multilocus sequence typing-based sequence type (ST), but the same RM system could be identified in diverse STs. The intra-ST conservation of ICR content suggests that this region may drive the emergence of new STs and promote clone stability. Sau3AI-like, LmoJ2 and LmoJ3 type II RM systems as well as type I EcoKI-like, and type IV AspBHI-like and <i>mcrB</i>-like systems accounted for all RM systems in the ICR. A Sau3AI-like type II RM system with specificity for GATC was harbored in the ICR of many STs, including all strains of the ancient, ubiquitous ST1. The extreme paucity of GATC recognition sites in lytic phages may reflect ancient adaptation of these phages to preempt resistance associated with the widely distributed Sau3AI-like systems. These findings indicate that the ICR has a high propensity for RM systems which are intraclonaly conserved and may impact bacteriophage susceptibility as well as ST emergence and stability.https://www.mdpi.com/2076-2607/11/3/699<i>Listeria</i>restriction modification systemimmigration control regionwhole genome sequencingchromosomal hotspot |
| spellingShingle | Phillip Brown Sangmi Lee Driss Elhanafi Wilhelm Tham Marie-Louise Danielsson-Tham Gloria Lopez-Valladares Yi Chen Mirena Ivanova Pimlapas Leekitcharoenphon Sophia Kathariou Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation Microorganisms <i>Listeria</i> restriction modification system immigration control region whole genome sequencing chromosomal hotspot |
| title | Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation |
| title_full | Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation |
| title_fullStr | Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation |
| title_full_unstemmed | Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation |
| title_short | Investigation of a <i>Listeria monocytogenes</i> Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation |
| title_sort | investigation of a i listeria monocytogenes i chromosomal immigration control region reveals diverse restriction modification systems with complete sequence type conservation |
| topic | <i>Listeria</i> restriction modification system immigration control region whole genome sequencing chromosomal hotspot |
| url | https://www.mdpi.com/2076-2607/11/3/699 |
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