AT Homopolymer Strings in Salmonella enterica Subspecies I Contribute to Speciation and Serovar Diversity
Abstract
:1. Introduction
Additional Background on Poultry-Associated S. enterica Serovars
2. Materials and Methods
2.1. Salmonella enterica Subspecies I Strains Analyzed for Strings of Homopolymers
2.2. Other Bacteria Analyzed for Comparison to S. enterica
2.3. Statistical Analysis of Kmer Content
2.4. Locating AT 8+Mers within Mutated Genes
3. Results
3.1. Homopolymer Strings of at Least 8 Nucleotides Were Dispersed in the Genome of S. enterica
3.2. The AT 8+mer Motif in Bacteria Was Specific to Genus and Species
3.3. The AT 8+mer Motif in the Chromosome Is Not Specific to Serovar
3.4. Characterization of the AT 8+mer Motif in Poultry-Associated Serovars of Salmonella
3.5. Location of AT 8+mers within Mutated Open Reading Frames
3.6. S. enterica Plasmids Have AT 8+mer Motifs Possibly Associated with Serovar Preference
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Phylum | Genus Species 1 | Other Genome Information | Number of Genomes Analyzed | Characteristics | Genome Size (bp) | Common Denominator (nt) 2 | Expected Number of 8+kmers | Observed AT 8+mers | Observed GC 8+mers | Observed vs. Expecterd AT 8+mers 3 | Observed vs. Expected GC 8+mers 3 |
---|---|---|---|---|---|---|---|---|---|---|---|
Proteobacteria | Salmonella enterica | Typhimurium | 12 | Average | 4,890,448 | 16,299 | 300.0 | 332.6 | 17.2 | 1.11 | 0.06 |
stdev | 50,356 | --- | 3.1 | 13.0 | 3.6 | --- | --- | ||||
Proteobacteria | Salmonella enterica | Enteritidis | 12 | Average | 4,686,462 | 16,299 | 287.5 | 323.7 | 21.5 | 1.13 | 0.07 |
stdev | 20,384 | --- | 1.3 | 10.5 | 4.2 | --- | --- | ||||
Proteobacteria | Salmonella enterica | Typhi | 12 | Average | 4,770,414 | 16,299 | 292.7 | 316.9 | 29.5 | 1.08 | 0.10 |
stdev | 60,270 | --- | 3.7 | 5.9 | 3.2 | --- | --- | ||||
Proteobacteria | Salmonella enterica | mixed | 12 | Average | 4,713,701 | 16,299 | 289.2 | 315.6 | 17.2 | 1.09 | 0.06 |
stdev | 80,652 | --- | 4.9 | 13.9 | 4.4 | --- | --- | ||||
Proteobacteria | Escherichia coli | --- | 12 | Average | 5,087,133 | 16,299 | 312.1 | 281.9 | 18.3 | 0.90 | 0.06 |
stdev | 262,098 | --- | 16.1 | 30.2 | 6.5 | --- | --- | ||||
Proteobacteria | Proteus mirabilis | --- | 3 | Average | 4,124,431 | 16,299 | 253.0 | 712.7 | 15.7 | 2.82 | 0.06 |
stdev | 83,305 | --- | 5.1 | 42.0 | 2.1 | --- | --- | ||||
Proteobacteria | Shigella sonnei | --- | 3 | Average | 4,929,599 | 16,299 | 302.4 | 261.3 | 11.7 | 0.86 | 0.04 |
stdev | 90,607 | --- | 5.6 | 8.4 | 3.5 | --- | --- | ||||
Proteobacteria | Yersinia pseudotuberculosis | --- | 3 | Average | 4,802,245 | 16,299 | 294.6 | 429.3 | 120.3 | 1.46 | 0.41 |
stdev | 118,706 | --- | 7.3 | 2.3 | 3.8 | --- | --- | ||||
Proteobacteria | Vibrio vulnificus | chromosome I | 3 | Average | 3,330,104 | 16,299 | 204.3 | 180.0 | 10.3 | 0.88 | 0.05 |
stdev | 79,423 | --- | 4.9 | 14.0 | 4.9 | --- | --- | ||||
Proteobacteria | Vibrio vulnificus | chromosome II | 3 | Average | 1,756,668 | 16,299 | 107.8 | 90.0 | 3.3 | 0.83 | 0.03 |
stdev | 87,177 | --- | 5.3 | 7.9 | 3.1 | --- | --- | ||||
Firmicutes | Staphylococcus aureus | --- | 3 | Average | 2,948,373 | 16,299 | 180.9 | 108.3 | 0.0 | 0.60 | 0.00 |
stdev | 114,371 | --- | 7.0 | 10.6 | 0.0 | --- | --- | ||||
Firmicutes | Streptococcus pyogenes | --- | 3 | Average | 1,895,707 | 16,299 | 116.3 | 263.7 | 0.3 | 2.27 | 0.00 |
stdev | 42,370 | --- | 2.6 | 15.4 | 0.6 | --- | --- | ||||
Firmicutes | Enterococcus faecalis | --- | 3 | Average | 3,090,387 | 16,299 | 189.6 | 649.7 | 2.0 | 3.42 | 0.01 |
stdev | 117,259 | --- | 7.2 | 84.1 | 3.5 | --- | --- | ||||
Firmicutes | Bacillus anthracis | --- | 3 | Average | 5,228,732 | 16,299 | 320.8 | 432.0 | 1.3 | 1.35 | 0.00 |
stdev | 1349 | --- | 0.1 | 11.5 | 0.6 | --- | --- | ||||
Firmicutes | Bacillus cereus | --- | 3 | Average | 5,406,060 | 16,299 | 331.7 | 700.3 | 13.0 | 2.11 | 0.04 |
stdev | 16,615 | --- | 1.0 | 53.7 | 6.1 | --- | --- |
STM Gene Accession | SEEG Gene Accession | SEN Gene Accession | AT 8+mer Sequence | Common Name of Gene | Description of Target Gene | Gene Function | Biological Process |
---|---|---|---|---|---|---|---|
no homolog | SEEG9184_21515 | SEN_RS22080 | conserved (3 locations) | sefC | SEEG pseudogene | Has 3 AT 8mers in sequence; outer membrane fimbrial protein SefC, pseudo in SG, which has an extra A/T to make a 7mer | adhesion |
STM0071 | SEEG9184_20585 | SEN_RS00360 | conserved | caiC | SEEG pseudogene | crotonobetaine/carnitine-CoA ligase | transporter |
STM0858 | SEEG9184_16520 | SEN_RS04155 | conserved | unnamed | SEEG pseudogene | electron transfer flavoprotein-ubiquinone oxidoreductase | transporter |
STM2020 | SEEG9184_10295 | SEN_RS10515 | conserved | cbiO | SEEG pseudogene | cobalt transport atp-binding protein CbiO: B12 synthesis associated? Truncated, maybe shorter product? | transporter |
STM2241 | SEEG9184_09260 | SEN_RS11570 | conserved | sspH2 | SEEG pseudogene | E3 ubiquitin-protein ligase; induced by the SPI-2 regulatory ssrA/B | virulence factor |
STM2274 | SEEG9184_09070 | SEN_RS11735 | conserved | unnamed | SEEG pseudogene | MFS transporter | transporter |
STM2691 | SEEG9184_07115 | SEN_RS13585 | conserved | unnamed | SEEG pseudogene | type I secretion system permease/ATPase: TolC family OMP | virulence factor |
STM3658 | SEEG9184_00930 | SEN_RS18105 | conserved | yiaH | SEEG pseudogene | acetyltransferase | biosynthesis |
STM1054 | SEEG9184_09275 | SEN_RS23040 | conserved | unnamed | SEN pseudogene, SEEG 78 bp tRNA region | Gifsy-2 prophage protein in STM: GC rich region has a 7 bp deletion in SEN in a guanidine rich fragment, causing a frameshift; homology in SEEG to tRNA-pro | phage associated |
STM4039 | SEEG9184_23265 | SEN_RS24515 | conserved | unnamed | SEN, SEEG pseudogene | HO protein | inner membrane protein |
STM1666 | no homolog | SEN_RS07090 | conserved | unnamed | STM pseudogene, SEEG absent | STM has in-frame stop following codon 24; SEN, hypothetical protein | unknown |
STM1550 | no homolog | SEN_RS07790 | Deletion of 154 bp in SEN | unnamed | SEN pseudogene, SEEG absent | type II toxin-antitoxin system mRNA interferase toxin | cellular detoxification |
STM0341 | SEEG9184_19090&19095 | SEN_RS01660 | SEEG 1 bp deletion | unnamed | SEEG pseudogene or split into two genes | STM and SEN, putative inner membrane protein; SEEG, 2 transmembrane regulators | inner membrane protein |
STM1130 | SEEG9184_15700 | SEN_RS05135 | SEEG 1 bp deletion | unnamed | SEEG pseudogene | N-acetylneuraminic acid mutarotase | metabolism |
STM1602 | SEEG9184_13085 | SEN_RS07535 | SEEG 1 bp deletion | sifB | SEEG pseudogene | effector protein SifB | virulence factor |
STM1698 | SEEG9184_13605 | SEN_RS06925 | SEEG 1 bp deletion | steC | SEEG pseudogene | secreted effector kinase SteC | virulence factor |
STM1869 | SEEG9184_14565 | SEN_RS06020 | SEEG 1 bp deletion | unnamed | SEEG pseudogene | HO protein | phage associated |
STM1939 | SEEG9184_15200 | SEN_RS05535 | SEEG 1 bp deletion | unnamed | SEEG pseudogene | putative glucose-6-phosphate dehydrogenase | metabolism |
STM2129 | SEEG9184_09800 | SEN_RS11065 | SEEG 1 bp deletion | yegB | SEEG pseudogene | multidrug transporter subunit MdtD | transporter |
no homolog | SEEG9184_21510 | SEN_RS22085 | SEEG 1 bp substitution | sefD | SEEG pseudogene | adhesin and master global regulator of phase transition; often mutated in SEN due to 1bp del in adenine homopolymer 8mer | regulon, adhesion |
STM1941 | SEEG9184_15210 | SEN_RS05525 | SEEG, SEN 1 bp deletion | unnamed | SEN, SEEG pseudogene | HO protein | inner membrane protein |
STM3674 | SEEG9184_00845 | SEN_RS18190 | SEEG, SEN 1 bp substitution | lyxK | SEEG pseudogene | carbohydrate kinase | metabolism |
Serovar | Typhimurium | Enteritidis | Gallinarum | Other Information | ||
---|---|---|---|---|---|---|
Accession | NC_003277.2 | NZ_CP063701.1 | CM001154.1 | |||
Other Name | pSLT | pSENV | str. SG9 | |||
Atmer Size | Description of Loci | Variation from pSLT | Variation from pSLT | pSLT Start | pSLT End | Gene Function |
9mer | Intergenic(PSLT039-PSLT038) | 1nt deletion | 1nt deletion | 27961 | 27969 | spvB-spvC;58nt upstream from spvC start |
10mer | Intergenic (PSLT041-PSLT042) | 1nt deletion | 2nt deletion | 32324 | 32333 | spvR-PSLT041: 10nt upstream from spvR start |
9mer | PSLT076 | present | absent | 62299 | 62307 | traY: conjugative transfer: oriT nicking |
8mer | PSLT088 | absent | present | 69093 | 69100 | traC: conjugative transfer: assembly |
8mer | PSLT102 | absent | absent | 82835 | 82842 | traS: conjugative transfer: surface exclusion |
8mer | PSLT111 | truncated | truncated | 93512 | 93519 | finO: conjugative transfer: regulation |
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Guard, J.; Rivers, A.R.; Vaughn, J.N.; Rothrock, Jr., M.J.; Oladeinde, A.; Shah, D.H. AT Homopolymer Strings in Salmonella enterica Subspecies I Contribute to Speciation and Serovar Diversity. Microorganisms 2021, 9, 2075. https://doi.org/10.3390/microorganisms9102075
Guard J, Rivers AR, Vaughn JN, Rothrock, Jr. MJ, Oladeinde A, Shah DH. AT Homopolymer Strings in Salmonella enterica Subspecies I Contribute to Speciation and Serovar Diversity. Microorganisms. 2021; 9(10):2075. https://doi.org/10.3390/microorganisms9102075
Chicago/Turabian StyleGuard, Jean, Adam R. Rivers, Justin N. Vaughn, Michael J. Rothrock, Jr., Adelumola Oladeinde, and Devendra H. Shah. 2021. "AT Homopolymer Strings in Salmonella enterica Subspecies I Contribute to Speciation and Serovar Diversity" Microorganisms 9, no. 10: 2075. https://doi.org/10.3390/microorganisms9102075
APA StyleGuard, J., Rivers, A. R., Vaughn, J. N., Rothrock, Jr., M. J., Oladeinde, A., & Shah, D. H. (2021). AT Homopolymer Strings in Salmonella enterica Subspecies I Contribute to Speciation and Serovar Diversity. Microorganisms, 9(10), 2075. https://doi.org/10.3390/microorganisms9102075