The number of Salmonella infection cases linked to pork products has increased. Pathogen presence in the feed mill environment is one of the many potential transmission routes into the food production chain.
ABSTRACT
The number of Salmonella infection cases linked to pork products has increased. Pathogen presence in the feed mill environment is one of the many potential transmission routes into the food production chain. Here, we describe the draft genome sequences of 57 Salmonella enterica isolates from selected U.S. swine feed mills.
ANNOUNCEMENT
Salmonella enterica, one of the most important pathogens in the food industry, is the leading cause of bacterial foodborne disease in the United States (1). While the impact on human health alone is enormous, there are also substantial economic repercussions of Salmonella outbreaks across the food industry. Therefore, it is important to have molecular typing data for well-characterized isolates from various sources. Whole-genome sequencing (WGS) has been increasingly used to characterize food and clinical Salmonella isolates (2).
Here, we describe the draft genome sequences of 57 S. enterica isolates collected during 2016 and 2017 from 11 U.S. swine feed mills (from 8 U.S. states) producing mash feed and/or pelleted feed (3). Within each mill, 12 sites were sampled, as follows: floor surfaces (n = 5), equipment (n = 4), brooms (n = 1), worker shoes (n = 1), and finished feed (n = 1). Samples were analyzed following the USDA Food Safety and Inspection Service (USDA-FSIS) guidelines (4), and identification was confirmed by PCR (5). Overnight tryptone soy broth cultures of positive isolates were subjected to DNA extraction using the DNeasy blood and tissue kit (Qiagen, Hilden, Germany). Paired-end DNA libraries were prepared with the Nextera XT DNA library preparation kit, and WGS was carried out on either a MiSeq or NextSeq sequencer, using a 500-cycle MiSeq reagent V2 kit or a 300-cycle NextSeq 500/550 high-output V2 kit, respectively (Illumina, San Diego, CA). Unless otherwise noted, default parameters were used in all analyses. De novo genome assemblies were obtained with the Shovill pipeline version 0.9 (https://github.com/tseemann/shovill), available in the GalaxyTrakr pipeline (https://www.galaxytrakr.org; see reference 6). The “trim reads” option was selected, and 500 bp was set as the minimum contig length. ResFinder and SPIFinder from the Center for Genomic Epidemiology were used to identify antibiotic resistance (AMR) genes and Salmonella pathogenicity islands (SPIs) in the draft genomes, respectively (https://cge.cbs.dtu.dk/services/). Draft genomes were annotated using the NCBI’s Prokaryotic Genome Annotation Pipeline (7). Salmonella serotypes were predicted from draft genomes with SeqSero 1.0 (http://www.denglab.info/SeqSero; see reference 8). Draft genomes ranged between 4,484,198 and 5,116,995 Mb in size, with 52% average GC content. The number of contigs for each isolate ranged from 29 to 86. The isolates belonged to 15 different serotypes, namely, Salmonella enterica serotypes Agona (n = 14), Mbandaka (n = 13), Senftenberg (n = 7), Schwarzengrund (n = 6), Rissen (n = 3), and Hartford and Typhimurium (n = 2 each). Nine serotypes were observed in only one isolate each, Salmonella enterica serotypes Bareilly, Braenderup, Cubana, Javiana, Kiambu, Poona, Soerenga, Worthington, and the potential monophasic variant of S. enterica serotype Typhimurium (I 4,[5],12:i:−). AMR genes were detected in 30 out of 57 strains, including those encoding tetracycline, phenicol, aminoglycoside, and beta-lactam resistance. Up to 12 SPIs were detected in these genomes, including SPI-1, SPI-2 and SPI-4, which encode predicted type I and type III secretion systems (9). The described draft genome sequences will be useful in comparative genomic analyses of S. enterica from the pork production chain in terms of phylogenetic insights into their evolution and support of further epidemiological investigations of outbreaks.
Data availability.
This whole-genome shotgun project has been deposited in DDBJ/ENA/GenBank under accession numbers QUTN00000000 to QUVQ00000000 and QUZX00000000 (Table 1). The first versions (QUTN01000000 to QUVQ01000000 and QUZX01000000) are described here.
TABLE 1.
Metadata for the 57 Salmonella enterica strains isolated from different feed mills in the United States between 2016 and 2017
| Sample identifier | BioSample no. | Run no. | Accession no. | No. of contigs |
Total length (bp) |
N50 (bp) | GC content (%) |
Genome coverage (×) |
|---|---|---|---|---|---|---|---|---|
| CFSAN071932 | SAMN08057838 | SRR6959189 | QUTN00000000 | 52 | 5,012,146 | 260,770 | 51.8 | 71 |
| CFSAN071933 | SAMN08057839 | SRR6959212 | QUTO00000000 | 49 | 5,010,824 | 235,309 | 51.8 | 91 |
| CFSAN071934 | SAMN08057843 | SRR6957504 | QUTP00000000 | 49 | 5,010,127 | 260,945 | 51.8 | 89 |
| CFSAN071935 | SAMN08057815 | SRR6957525 | QUTQ00000000 | 86 | 5,116,995 | 271,078 | 52.1 | 135 |
| CFSAN071936 | SAMN08057823 | SRR6959053 | QUTR00000000 | 56 | 4,974,144 | 235,297 | 51.8 | 123 |
| CFSAN071937 | SAMN08057820 | SRR6959057 | QUTS00000000 | 39 | 4,780,443 | 292,436 | 52.1 | 148 |
| CFSAN071938 | SAMN08057858 | SRR6959072 | QUTT00000000 | 43 | 4,782,578 | 268,283 | 52.1 | 133 |
| CFSAN071940 | SAMN08057866 | SRR6959115 | QUTU00000000 | 41 | 4,484,295 | 381,546 | 52.2 | 112 |
| CFSAN071941 | SAMN08057869 | SRR6958537 | QUTV00000000 | 39 | 4,484,198 | 381,546 | 52.2 | 139 |
| CFSAN071943 | SAMN08057863 | SRR7545387 | QUTW00000000 | 36 | 4,943,381 | 341,411 | 51.8 | 135 |
| CFSAN071944 | SAMN08057865 | SRR6957683 | QUTX00000000 | 56 | 4,797,481 | 381,076 | 52.2 | 139 |
| CFSAN071945 | SAMN08057879 | SRR6959319 | QUTY00000000 | 61 | 4,689,856 | 236,673 | 52.1 | 127 |
| CFSAN071946 | SAMN08057880 | SRR6959315 | QUTZ00000000 | 45 | 4,973,164 | 389,983 | 52 | 139 |
| CFSAN071947 | SAMN08057876 | SRR6959018 | QUUA00000000 | 39 | 4,974,888 | 390,021 | 52 | 154 |
| CFSAN071948 | SAMN08057877 | SRR6959052 | QUUB00000000 | 43 | 4,672,093 | 235,297 | 52.2 | 74 |
| CFSAN071949 | SAMN08057888 | SRR6958605 | QUUC00000000 | 40 | 4,974,485 | 412,899 | 52 | 140 |
| CFSAN071950 | SAMN08057887 | SRR6958972 | QUUD00000000 | 50 | 4,971,687 | 317,512 | 52 | 127 |
| CFSAN071951 | SAMN08057883 | SRR6957691 | QUUE00000000 | 39 | 4,978,782 | 412,745 | 52 | 51 |
| CFSAN071952 | SAMN08057882 | SRR6959190 | QUUF00000000 | 42 | 4,830,818 | 401,049 | 52.2 | 186 |
| CFSAN071953 | SAMN08057886 | SRR6959322 | QUUG00000000 | 53 | 4,689,837 | 278,573 | 52.1 | 164 |
| CFSAN071954 | SAMN08057885 | SRR6959202 | QUUH00000000 | 29 | 4,780,916 | 408,171 | 52 | 164 |
| CFSAN071955 | SAMN08057836 | SRR6959274 | QUUI00000000 | 33 | 4,707,452 | 389,545 | 52.1 | 125 |
| CFSAN071956 | SAMN08057825 | SRR6958149 | QUUJ00000000 | 58 | 4,696,591 | 245,410 | 52.1 | 160 |
| CFSAN071957 | SAMN08057821 | SRR6958145 | QUUK00000000 | 60 | 4,696,272 | 259,971 | 52.1 | 181 |
| CFSAN071958 | SAMN08057819 | SRR6958473 | QUUL00000000 | 57 | 4,690,445 | 259,968 | 52.1 | 182 |
| CFSAN071959 | SAMN08057816 | SRR6958470 | QUUM00000000 | 59 | 4,690,960 | 235,297 | 52.1 | 187 |
| CFSAN071960 | SAMN08057868 | SRR6958115 | QUUN00000000 | 45 | 4,813,521 | 322,240 | 52.2 | 187 |
| CFSAN071961 | SAMN08057881 | SRR6956165 | QUUO00000000 | 39 | 4,781,312 | 440,059 | 52.1 | 177 |
| CFSAN071964 | SAMN08057864 | SRR6957524 | QUUP00000000 | 38 | 4,721,388 | 363,871 | 52.1 | 127 |
| CFSAN071965 | SAMN08057889 | SRR6957526 | QUUQ00000000 | 74 | 4,978,222 | 214,013 | 52.1 | 133 |
| CFSAN071966 | SAMN08057809 | SRR6957442 | QUUR00000000 | 78 | 4,980,304 | 214,013 | 52.1 | 134 |
| CFSAN071967 | SAMN08057806 | SRR6956728 | QUUS00000000 | 67 | 4,936,335 | 146,406 | 52.1 | 117 |
| CFSAN071968 | SAMN08057804 | SRR6956712 | QUUT00000000 | 35 | 4,708,769 | 437,088 | 52.3 | 148 |
| CFSAN071969 | SAMN08057824 | SRR6956669 | QUUU00000000 | 46 | 4,780,193 | 267,610 | 52.1 | 144 |
| CFSAN071970 | SAMN08057822 | SRR6651925 | QUUV00000000 | 32 | 4,829,698 | 447,189 | 52.1 | 175 |
| CFSAN071971 | SAMN08057833 | SRR6653453 | QUUW00000000 | 34 | 4,827,673 | 447,721 | 52.1 | 182 |
| CFSAN071972 | SAMN08057832 | SRR6653448 | QUUX00000000 | 41 | 4,760,816 | 280,947 | 52 | 156 |
| CFSAN071973 | SAMN08057831 | SRR6651923 | QUUY00000000 | 55 | 5,010,453 | 350,213 | 51.8 | 143 |
| CFSAN071974 | SAMN08057842 | SRR6653464 | QUUZ00000000 | 54 | 4,994,979 | 307,967 | 51.8 | 146 |
| CFSAN071975 | SAMN08057848 | SRR6653465 | QUVA00000000 | 51 | 4,994,206 | 307,967 | 51.8 | 125 |
| CFSAN071976 | SAMN08057856 | SRR6654229 | QUVB00000000 | 48 | 4,994,668 | 360,164 | 51.8 | 194 |
| CFSAN071977 | SAMN08057857 | SRR6654195 | QUVC00000000 | 47 | 4,995,733 | 329,065 | 51.8 | 212 |
| CFSAN071978 | SAMN08057853 | SRR6654125 | QUVD00000000 | 55 | 5,008,977 | 350,306 | 51.8 | 189 |
| CFSAN071979 | SAMN08057849 | SRR6654123 | QUVE00000000 | 50 | 4,996,561 | 307,967 | 51.8 | 181 |
| CFSAN071980 | SAMN08057850 | SRR6651152 | QUVF00000000 | 50 | 5,007,268 | 307,967 | 51.8 | 231 |
| CFSAN071981 | SAMN08057847 | SRR6651155 | QUVG00000000 | 56 | 5,009,733 | 307,967 | 51.8 | 208 |
| CFSAN071982 | SAMN08057855 | SRR6651156 | QUVH00000000 | 49 | 4,994,374 | 360,164 | 51.8 | 228 |
| CFSAN071983 | SAMN08057854 | SRR6650949 | QUVI00000000 | 50 | 4,995,973 | 307,793 | 51.8 | 227 |
| CFSAN071984 | SAMN08057851 | SRR6650951 | QUVJ00000000 | 54 | 5,008,558 | 350,213 | 51.8 | 143 |
| CFSAN071985 | SAMN08057871 | SRR6651157 | QUVK00000000 | 52 | 5,010,076 | 328,176 | 51.8 | 164 |
| CFSAN071986 | SAMN08057870 | SRR6650950 | QUVL00000000 | 55 | 5,008,380 | 307,967 | 51.8 | 129 |
| CFSAN071990 | SAMN08057875 | SRR6958062 | QUVM00000000 | 41 | 4,745,986 | 454,049 | 52.2 | 110 |
| CFSAN071991 | SAMN08057874 | SRR6957337 | QUVN00000000 | 51 | 4,835,035 | 246,700 | 52.1 | 48 |
| CFSAN071992 | SAMN08057873 | SRR7771352 | QUVO00000000 | 47 | 4,843,802 | 262,144 | 52.1 | 88 |
| CFSAN071993 | SAMN08057805 | SRR6958582 | QUVP00000000 | 37 | 4,794,792 | 281,696 | 52 | 74 |
| CFSAN071994 | SAMN08057807 | SRR6957350 | QUVQ00000000 | 39 | 4,794,849 | 276,964 | 52 | 128 |
| CFSAN074091 | SAMN09695778 | SRR7545388 | QUZX00000000 | 41 | 4,974,987 | 412,331 | 52 | 322 |
ACKNOWLEDGMENTS
This work was supported by the Center for Food Safety and Applied Nutrition (CFSAN) at the U.S. Food and Drug Administration (FDA). This project was also supported in part by an appointment to the Research Participation Program at the CFSAN, U.S. FDA, administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and the FDA.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the U.S. FDA. The use of trade names and commercial sources is for identification purposes only and does not imply endorsement.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
This whole-genome shotgun project has been deposited in DDBJ/ENA/GenBank under accession numbers QUTN00000000 to QUVQ00000000 and QUZX00000000 (Table 1). The first versions (QUTN01000000 to QUVQ01000000 and QUZX01000000) are described here.
TABLE 1.
Metadata for the 57 Salmonella enterica strains isolated from different feed mills in the United States between 2016 and 2017
| Sample identifier | BioSample no. | Run no. | Accession no. | No. of contigs |
Total length (bp) |
N50 (bp) | GC content (%) |
Genome coverage (×) |
|---|---|---|---|---|---|---|---|---|
| CFSAN071932 | SAMN08057838 | SRR6959189 | QUTN00000000 | 52 | 5,012,146 | 260,770 | 51.8 | 71 |
| CFSAN071933 | SAMN08057839 | SRR6959212 | QUTO00000000 | 49 | 5,010,824 | 235,309 | 51.8 | 91 |
| CFSAN071934 | SAMN08057843 | SRR6957504 | QUTP00000000 | 49 | 5,010,127 | 260,945 | 51.8 | 89 |
| CFSAN071935 | SAMN08057815 | SRR6957525 | QUTQ00000000 | 86 | 5,116,995 | 271,078 | 52.1 | 135 |
| CFSAN071936 | SAMN08057823 | SRR6959053 | QUTR00000000 | 56 | 4,974,144 | 235,297 | 51.8 | 123 |
| CFSAN071937 | SAMN08057820 | SRR6959057 | QUTS00000000 | 39 | 4,780,443 | 292,436 | 52.1 | 148 |
| CFSAN071938 | SAMN08057858 | SRR6959072 | QUTT00000000 | 43 | 4,782,578 | 268,283 | 52.1 | 133 |
| CFSAN071940 | SAMN08057866 | SRR6959115 | QUTU00000000 | 41 | 4,484,295 | 381,546 | 52.2 | 112 |
| CFSAN071941 | SAMN08057869 | SRR6958537 | QUTV00000000 | 39 | 4,484,198 | 381,546 | 52.2 | 139 |
| CFSAN071943 | SAMN08057863 | SRR7545387 | QUTW00000000 | 36 | 4,943,381 | 341,411 | 51.8 | 135 |
| CFSAN071944 | SAMN08057865 | SRR6957683 | QUTX00000000 | 56 | 4,797,481 | 381,076 | 52.2 | 139 |
| CFSAN071945 | SAMN08057879 | SRR6959319 | QUTY00000000 | 61 | 4,689,856 | 236,673 | 52.1 | 127 |
| CFSAN071946 | SAMN08057880 | SRR6959315 | QUTZ00000000 | 45 | 4,973,164 | 389,983 | 52 | 139 |
| CFSAN071947 | SAMN08057876 | SRR6959018 | QUUA00000000 | 39 | 4,974,888 | 390,021 | 52 | 154 |
| CFSAN071948 | SAMN08057877 | SRR6959052 | QUUB00000000 | 43 | 4,672,093 | 235,297 | 52.2 | 74 |
| CFSAN071949 | SAMN08057888 | SRR6958605 | QUUC00000000 | 40 | 4,974,485 | 412,899 | 52 | 140 |
| CFSAN071950 | SAMN08057887 | SRR6958972 | QUUD00000000 | 50 | 4,971,687 | 317,512 | 52 | 127 |
| CFSAN071951 | SAMN08057883 | SRR6957691 | QUUE00000000 | 39 | 4,978,782 | 412,745 | 52 | 51 |
| CFSAN071952 | SAMN08057882 | SRR6959190 | QUUF00000000 | 42 | 4,830,818 | 401,049 | 52.2 | 186 |
| CFSAN071953 | SAMN08057886 | SRR6959322 | QUUG00000000 | 53 | 4,689,837 | 278,573 | 52.1 | 164 |
| CFSAN071954 | SAMN08057885 | SRR6959202 | QUUH00000000 | 29 | 4,780,916 | 408,171 | 52 | 164 |
| CFSAN071955 | SAMN08057836 | SRR6959274 | QUUI00000000 | 33 | 4,707,452 | 389,545 | 52.1 | 125 |
| CFSAN071956 | SAMN08057825 | SRR6958149 | QUUJ00000000 | 58 | 4,696,591 | 245,410 | 52.1 | 160 |
| CFSAN071957 | SAMN08057821 | SRR6958145 | QUUK00000000 | 60 | 4,696,272 | 259,971 | 52.1 | 181 |
| CFSAN071958 | SAMN08057819 | SRR6958473 | QUUL00000000 | 57 | 4,690,445 | 259,968 | 52.1 | 182 |
| CFSAN071959 | SAMN08057816 | SRR6958470 | QUUM00000000 | 59 | 4,690,960 | 235,297 | 52.1 | 187 |
| CFSAN071960 | SAMN08057868 | SRR6958115 | QUUN00000000 | 45 | 4,813,521 | 322,240 | 52.2 | 187 |
| CFSAN071961 | SAMN08057881 | SRR6956165 | QUUO00000000 | 39 | 4,781,312 | 440,059 | 52.1 | 177 |
| CFSAN071964 | SAMN08057864 | SRR6957524 | QUUP00000000 | 38 | 4,721,388 | 363,871 | 52.1 | 127 |
| CFSAN071965 | SAMN08057889 | SRR6957526 | QUUQ00000000 | 74 | 4,978,222 | 214,013 | 52.1 | 133 |
| CFSAN071966 | SAMN08057809 | SRR6957442 | QUUR00000000 | 78 | 4,980,304 | 214,013 | 52.1 | 134 |
| CFSAN071967 | SAMN08057806 | SRR6956728 | QUUS00000000 | 67 | 4,936,335 | 146,406 | 52.1 | 117 |
| CFSAN071968 | SAMN08057804 | SRR6956712 | QUUT00000000 | 35 | 4,708,769 | 437,088 | 52.3 | 148 |
| CFSAN071969 | SAMN08057824 | SRR6956669 | QUUU00000000 | 46 | 4,780,193 | 267,610 | 52.1 | 144 |
| CFSAN071970 | SAMN08057822 | SRR6651925 | QUUV00000000 | 32 | 4,829,698 | 447,189 | 52.1 | 175 |
| CFSAN071971 | SAMN08057833 | SRR6653453 | QUUW00000000 | 34 | 4,827,673 | 447,721 | 52.1 | 182 |
| CFSAN071972 | SAMN08057832 | SRR6653448 | QUUX00000000 | 41 | 4,760,816 | 280,947 | 52 | 156 |
| CFSAN071973 | SAMN08057831 | SRR6651923 | QUUY00000000 | 55 | 5,010,453 | 350,213 | 51.8 | 143 |
| CFSAN071974 | SAMN08057842 | SRR6653464 | QUUZ00000000 | 54 | 4,994,979 | 307,967 | 51.8 | 146 |
| CFSAN071975 | SAMN08057848 | SRR6653465 | QUVA00000000 | 51 | 4,994,206 | 307,967 | 51.8 | 125 |
| CFSAN071976 | SAMN08057856 | SRR6654229 | QUVB00000000 | 48 | 4,994,668 | 360,164 | 51.8 | 194 |
| CFSAN071977 | SAMN08057857 | SRR6654195 | QUVC00000000 | 47 | 4,995,733 | 329,065 | 51.8 | 212 |
| CFSAN071978 | SAMN08057853 | SRR6654125 | QUVD00000000 | 55 | 5,008,977 | 350,306 | 51.8 | 189 |
| CFSAN071979 | SAMN08057849 | SRR6654123 | QUVE00000000 | 50 | 4,996,561 | 307,967 | 51.8 | 181 |
| CFSAN071980 | SAMN08057850 | SRR6651152 | QUVF00000000 | 50 | 5,007,268 | 307,967 | 51.8 | 231 |
| CFSAN071981 | SAMN08057847 | SRR6651155 | QUVG00000000 | 56 | 5,009,733 | 307,967 | 51.8 | 208 |
| CFSAN071982 | SAMN08057855 | SRR6651156 | QUVH00000000 | 49 | 4,994,374 | 360,164 | 51.8 | 228 |
| CFSAN071983 | SAMN08057854 | SRR6650949 | QUVI00000000 | 50 | 4,995,973 | 307,793 | 51.8 | 227 |
| CFSAN071984 | SAMN08057851 | SRR6650951 | QUVJ00000000 | 54 | 5,008,558 | 350,213 | 51.8 | 143 |
| CFSAN071985 | SAMN08057871 | SRR6651157 | QUVK00000000 | 52 | 5,010,076 | 328,176 | 51.8 | 164 |
| CFSAN071986 | SAMN08057870 | SRR6650950 | QUVL00000000 | 55 | 5,008,380 | 307,967 | 51.8 | 129 |
| CFSAN071990 | SAMN08057875 | SRR6958062 | QUVM00000000 | 41 | 4,745,986 | 454,049 | 52.2 | 110 |
| CFSAN071991 | SAMN08057874 | SRR6957337 | QUVN00000000 | 51 | 4,835,035 | 246,700 | 52.1 | 48 |
| CFSAN071992 | SAMN08057873 | SRR7771352 | QUVO00000000 | 47 | 4,843,802 | 262,144 | 52.1 | 88 |
| CFSAN071993 | SAMN08057805 | SRR6958582 | QUVP00000000 | 37 | 4,794,792 | 281,696 | 52 | 74 |
| CFSAN071994 | SAMN08057807 | SRR6957350 | QUVQ00000000 | 39 | 4,794,849 | 276,964 | 52 | 128 |
| CFSAN074091 | SAMN09695778 | SRR7545388 | QUZX00000000 | 41 | 4,974,987 | 412,331 | 52 | 322 |