Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells
Abstract Background The impact of S. enterica colonization in cattle is highly variable and often serovar-dependent. The aim of this study was to compare the global transcriptomes of highly pathogenic bovine-adapted S. enterica serovar Dublin and the less pathogenic, bovine-adapted, serovar Cerro du...
Main Authors: | , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2022-07-01
|
Series: | BMC Genomics |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12864-022-08725-z |
_version_ | 1811323583643779072 |
---|---|
author | Serajus Salaheen Seon Woo Kim Bradd J. Haley Jo Ann S. Van Kessel |
author_facet | Serajus Salaheen Seon Woo Kim Bradd J. Haley Jo Ann S. Van Kessel |
author_sort | Serajus Salaheen |
collection | DOAJ |
description | Abstract Background The impact of S. enterica colonization in cattle is highly variable and often serovar-dependent. The aim of this study was to compare the global transcriptomes of highly pathogenic bovine-adapted S. enterica serovar Dublin and the less pathogenic, bovine-adapted, serovar Cerro during interactions with bovine epithelial cells, to identify genes that impact serovar-related outcomes of S. enterica infections in dairy animals. Result Bovine epithelial cells were infected with S. enterica strains from serovars Dublin and Cerro, and the bacterial RNA was extracted and sequenced. The total number of paired-end reads uniquely mapped to non-rRNA and non-tRNA genes in the reference genomes ranged between 12.1 M (Million) and 23.4 M (median: 15.7 M). In total, 360 differentially expressed genes (DEGs) were identified with at least two-fold differences in the transcript abundances between S. Dublin and S. Cerro (false discovery rate ≤ 5%). The highest number of DEGs (17.5%, 63 of 360 genes) between the two serovars were located on the genomic regions potentially associated with Salmonella Pathogenicity Islands (SPIs). DEGs potentially located in the SPI-regions that were upregulated (≥ 2-fold) in the S. Dublin compared with S. Cerro included: 37 SPI-1 genes encoding mostly Type 3 Secretion System (T3SS) apparatus and effectors; all of the six SPI-4 genes encoding type I secretion apparatus (siiABCDEF); T3SS effectors and chaperone (sopB, pipB, and sigE) located in SPI-5; type VI secretion system associated protein coding genes (sciJKNOR) located in SPI-6; and T3SS effector sopF in SPI-11. Additional major functional categories of DEGs included transcription regulators (n = 25), amino acid transport and metabolism (n = 20), carbohydrate transport and metabolism (n = 20), energy production and metabolism (n = 19), cell membrane biogenesis (n = 18), and coenzyme transport and metabolism (n = 15). DEGs were further mapped to the metabolic pathways listed in the KEGG database; most genes of the fatty acid β-oxidation pathway were upregulated/uniquely present in the S. Dublin strains compared with the S. Cerro strains. Conclusions This study identified S. enterica genes that may be responsible for symptomatic or asymptomatic infection and colonization of two bovine-adapted serovars in cattle. |
first_indexed | 2024-04-13T13:57:47Z |
format | Article |
id | doaj.art-8f3b67a24683460d9e17d2f6464276b3 |
institution | Directory Open Access Journal |
issn | 1471-2164 |
language | English |
last_indexed | 2024-04-13T13:57:47Z |
publishDate | 2022-07-01 |
publisher | BMC |
record_format | Article |
series | BMC Genomics |
spelling | doaj.art-8f3b67a24683460d9e17d2f6464276b32022-12-22T02:44:08ZengBMCBMC Genomics1471-21642022-07-0123111110.1186/s12864-022-08725-zDifferences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cellsSerajus Salaheen0Seon Woo Kim1Bradd J. Haley2Jo Ann S. Van Kessel3Environmental Microbial and Food Safety Laboratory, Beltsville Agricultural Research Center, USDA-ARSEnvironmental Microbial and Food Safety Laboratory, Beltsville Agricultural Research Center, USDA-ARSEnvironmental Microbial and Food Safety Laboratory, Beltsville Agricultural Research Center, USDA-ARSEnvironmental Microbial and Food Safety Laboratory, Beltsville Agricultural Research Center, USDA-ARSAbstract Background The impact of S. enterica colonization in cattle is highly variable and often serovar-dependent. The aim of this study was to compare the global transcriptomes of highly pathogenic bovine-adapted S. enterica serovar Dublin and the less pathogenic, bovine-adapted, serovar Cerro during interactions with bovine epithelial cells, to identify genes that impact serovar-related outcomes of S. enterica infections in dairy animals. Result Bovine epithelial cells were infected with S. enterica strains from serovars Dublin and Cerro, and the bacterial RNA was extracted and sequenced. The total number of paired-end reads uniquely mapped to non-rRNA and non-tRNA genes in the reference genomes ranged between 12.1 M (Million) and 23.4 M (median: 15.7 M). In total, 360 differentially expressed genes (DEGs) were identified with at least two-fold differences in the transcript abundances between S. Dublin and S. Cerro (false discovery rate ≤ 5%). The highest number of DEGs (17.5%, 63 of 360 genes) between the two serovars were located on the genomic regions potentially associated with Salmonella Pathogenicity Islands (SPIs). DEGs potentially located in the SPI-regions that were upregulated (≥ 2-fold) in the S. Dublin compared with S. Cerro included: 37 SPI-1 genes encoding mostly Type 3 Secretion System (T3SS) apparatus and effectors; all of the six SPI-4 genes encoding type I secretion apparatus (siiABCDEF); T3SS effectors and chaperone (sopB, pipB, and sigE) located in SPI-5; type VI secretion system associated protein coding genes (sciJKNOR) located in SPI-6; and T3SS effector sopF in SPI-11. Additional major functional categories of DEGs included transcription regulators (n = 25), amino acid transport and metabolism (n = 20), carbohydrate transport and metabolism (n = 20), energy production and metabolism (n = 19), cell membrane biogenesis (n = 18), and coenzyme transport and metabolism (n = 15). DEGs were further mapped to the metabolic pathways listed in the KEGG database; most genes of the fatty acid β-oxidation pathway were upregulated/uniquely present in the S. Dublin strains compared with the S. Cerro strains. Conclusions This study identified S. enterica genes that may be responsible for symptomatic or asymptomatic infection and colonization of two bovine-adapted serovars in cattle.https://doi.org/10.1186/s12864-022-08725-zRNA-SeqSalmonellaSerovarS. DublinS. CerroEpithelial cells |
spellingShingle | Serajus Salaheen Seon Woo Kim Bradd J. Haley Jo Ann S. Van Kessel Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells BMC Genomics RNA-Seq Salmonella Serovar S. Dublin S. Cerro Epithelial cells |
title | Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells |
title_full | Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells |
title_fullStr | Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells |
title_full_unstemmed | Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells |
title_short | Differences between the global transcriptomes of Salmonella enterica serovars Dublin and Cerro infecting bovine epithelial cells |
title_sort | differences between the global transcriptomes of salmonella enterica serovars dublin and cerro infecting bovine epithelial cells |
topic | RNA-Seq Salmonella Serovar S. Dublin S. Cerro Epithelial cells |
url | https://doi.org/10.1186/s12864-022-08725-z |
work_keys_str_mv | AT serajussalaheen differencesbetweentheglobaltranscriptomesofsalmonellaentericaserovarsdublinandcerroinfectingbovineepithelialcells AT seonwookim differencesbetweentheglobaltranscriptomesofsalmonellaentericaserovarsdublinandcerroinfectingbovineepithelialcells AT braddjhaley differencesbetweentheglobaltranscriptomesofsalmonellaentericaserovarsdublinandcerroinfectingbovineepithelialcells AT joannsvankessel differencesbetweentheglobaltranscriptomesofsalmonellaentericaserovarsdublinandcerroinfectingbovineepithelialcells |