Cargando…
Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper
Low moisture foods (LMFs) have traditionally been recognized as safe for consumption, as most bacteria require higher water content to grow. However, outbreaks due to LMF foods are increasing, and the microbial pathogen Salmonella enterica is frequently implicated. S. enterica can survive in LMFs fo...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507087/ https://www.ncbi.nlm.nih.gov/pubmed/36160197 http://dx.doi.org/10.3389/fmicb.2022.970135 |
_version_ | 1784796841794076672 |
---|---|
author | Davies, Cary P. Jurkiw, Thomas Haendiges, Julie Reed, Elizabeth Anderson, Nathan Grasso-Kelley, Elizabeth Hoffmann, Maria Zheng, Jie |
author_facet | Davies, Cary P. Jurkiw, Thomas Haendiges, Julie Reed, Elizabeth Anderson, Nathan Grasso-Kelley, Elizabeth Hoffmann, Maria Zheng, Jie |
author_sort | Davies, Cary P. |
collection | PubMed |
description | Low moisture foods (LMFs) have traditionally been recognized as safe for consumption, as most bacteria require higher water content to grow. However, outbreaks due to LMF foods are increasing, and the microbial pathogen Salmonella enterica is frequently implicated. S. enterica can survive in LMFs for years, but few serovars have been studied, and the mechanisms which underlie this longevity are not well understood. Here, we determine that S. enterica serovars S. Tennessee, S. Anatum, and S. Reading but not S. Oranienburg can survive in the ground black pepper for 6 years. S. Reading was not previously associated with any LMF. Using both Illumina and Pacific Biosciences sequencing technologies, we also document changes in the genomes and methylomes of the surviving serovars over this 6-year period. The three serovars acquired a small number of single nucleotide polymorphisms (SNPs) including seven substitutions (four synonymous, two non-synonymous, and one substitution in a non-coding region), and two insertion-deletions. Nine distinct N6-methyladenine (m6A) methylated motifs across the three serovars were identified including five which were previously known, G(m6)ATC, CAG(m6)AG, BATGC(m6)AT, CRT(m6)AYN(6)CTC, and CC(m6)AN(7)TGAG, and four novel serovar-specific motifs, GRT(m6)AN(8)TTYG, GA(m6)ACN(7)GTA, GAA m(6A)CY, and CAA(m6)ANCC. Interestingly, the BATGCAT motif was incompletely methylated (35–64% sites across the genome methylated), suggesting a possible role in gene regulation. Furthermore, the number of methylated BATGC(m6)AT motifs increased after storage in ground black pepper for 6 years from 475 to 657 (S. Tennessee), 366 to 608 (S. Anatum), and 525 to 570 (S. Reading), thus warranting further study as an adaptive mechanism. This is the first long-term assessment of genomic changes in S. enterica in a low moisture environment, and the first study to examine the methylome of any bacteria over a period of years, to our knowledge. These data contribute to our understanding of S. enterica survival in LMFs, and coupled with further studies, will provide the information necessary to design effective interventions which reduce S. enterica in LMFs and maintain a healthy, safe food supply. |
format | Online Article Text |
id | pubmed-9507087 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-95070872022-09-24 Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper Davies, Cary P. Jurkiw, Thomas Haendiges, Julie Reed, Elizabeth Anderson, Nathan Grasso-Kelley, Elizabeth Hoffmann, Maria Zheng, Jie Front Microbiol Microbiology Low moisture foods (LMFs) have traditionally been recognized as safe for consumption, as most bacteria require higher water content to grow. However, outbreaks due to LMF foods are increasing, and the microbial pathogen Salmonella enterica is frequently implicated. S. enterica can survive in LMFs for years, but few serovars have been studied, and the mechanisms which underlie this longevity are not well understood. Here, we determine that S. enterica serovars S. Tennessee, S. Anatum, and S. Reading but not S. Oranienburg can survive in the ground black pepper for 6 years. S. Reading was not previously associated with any LMF. Using both Illumina and Pacific Biosciences sequencing technologies, we also document changes in the genomes and methylomes of the surviving serovars over this 6-year period. The three serovars acquired a small number of single nucleotide polymorphisms (SNPs) including seven substitutions (four synonymous, two non-synonymous, and one substitution in a non-coding region), and two insertion-deletions. Nine distinct N6-methyladenine (m6A) methylated motifs across the three serovars were identified including five which were previously known, G(m6)ATC, CAG(m6)AG, BATGC(m6)AT, CRT(m6)AYN(6)CTC, and CC(m6)AN(7)TGAG, and four novel serovar-specific motifs, GRT(m6)AN(8)TTYG, GA(m6)ACN(7)GTA, GAA m(6A)CY, and CAA(m6)ANCC. Interestingly, the BATGCAT motif was incompletely methylated (35–64% sites across the genome methylated), suggesting a possible role in gene regulation. Furthermore, the number of methylated BATGC(m6)AT motifs increased after storage in ground black pepper for 6 years from 475 to 657 (S. Tennessee), 366 to 608 (S. Anatum), and 525 to 570 (S. Reading), thus warranting further study as an adaptive mechanism. This is the first long-term assessment of genomic changes in S. enterica in a low moisture environment, and the first study to examine the methylome of any bacteria over a period of years, to our knowledge. These data contribute to our understanding of S. enterica survival in LMFs, and coupled with further studies, will provide the information necessary to design effective interventions which reduce S. enterica in LMFs and maintain a healthy, safe food supply. Frontiers Media S.A. 2022-09-09 /pmc/articles/PMC9507087/ /pubmed/36160197 http://dx.doi.org/10.3389/fmicb.2022.970135 Text en Copyright © 2022 Davies, Jurkiw, Haendiges, Reed, Anderson, Grasso-Kelley, Hoffmann and Zheng. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Davies, Cary P. Jurkiw, Thomas Haendiges, Julie Reed, Elizabeth Anderson, Nathan Grasso-Kelley, Elizabeth Hoffmann, Maria Zheng, Jie Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title | Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title_full | Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title_fullStr | Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title_full_unstemmed | Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title_short | Changes in the genomes and methylomes of three Salmonella enterica serovars after long-term storage in ground black pepper |
title_sort | changes in the genomes and methylomes of three salmonella enterica serovars after long-term storage in ground black pepper |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507087/ https://www.ncbi.nlm.nih.gov/pubmed/36160197 http://dx.doi.org/10.3389/fmicb.2022.970135 |
work_keys_str_mv | AT daviescaryp changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT jurkiwthomas changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT haendigesjulie changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT reedelizabeth changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT andersonnathan changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT grassokelleyelizabeth changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT hoffmannmaria changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper AT zhengjie changesinthegenomesandmethylomesofthreesalmonellaentericaserovarsafterlongtermstorageingroundblackpepper |