Whole Genome Sequencing and Comparative Genomics of Six Staphylococcus schleiferi and Staphylococcus coagulans Isolates
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains, Media, and Growth Conditions
2.2. DNA Extraction, Library Preparation, and Whole Genome Sequencing
2.3. Comparative Genomics Analysis
3. Results
3.1. Genomic Features of Human Staphylococcus schleiferi and Staphylococcus coagulans
3.2. Type-Based Species Clustering
3.3. Nucleotide Sequence Accession Numbers
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Yamashita, K.; Shimizu, A.; Kawano, J.; Uchida, E.; Haruna, A.; Igimi, S. Isolation and characterization of staphylococci from external auditory meatus of dogs with or without otitis externa with special reference to Staphylococcus schleiferi subsp. coagulans isolates. J. Vet. Med. Sci. 2005, 67, 263–268. [Google Scholar] [CrossRef]
- May, E.R.; Hnilica, K.A.; Frank, L.A.; Jones, R.D.; Bemis, D.A. Isolation of Staphylococcus schleiferi from healthy dogs and dogs with otitis, pyoderma, or both. J. Am. Vet. Med. Assoc. 2005, 227, 928–931. [Google Scholar] [CrossRef]
- Paterson, G.K. Genomic epidemiology of the opportunistic pathogen Staphylococcus coagulans from companion dogs. J. Med. Microbiol. 2021, 70, 001407. [Google Scholar] [CrossRef]
- Kumar, D.; Cawley, J.J.; Irizarry-Alvarado, J.M.; Alvarez, A.; Alvarez, S. Case of Staphylococcus schleiferi subspecies coagulans endocarditis and metastatic infection in an immune compromised host. Transpl. Infect Dis. 2007, 9, 336–338. [Google Scholar] [CrossRef]
- Igimi, S.; Takahashi, E.; Mitsuoka, T. Staphylococcus schleiferi subsp. coagulans subsp. nov., isolated from the external auditory meatus of dogs with external ear otitis. Int. J. Syst. Bacteriol. 1990, 40, 409–411. [Google Scholar] [CrossRef]
- Naing, S.Y.; Duim, B.; Broens, E.M.; Schweitzer, V.; Zomer, A.; van der Graaf-van Bloois, L.; van der Meer, C.; Stellingwerff, L.; Fluit, A.C.; Wagenaar, J.A. Molecular Characterization and Clinical Relevance of Taxonomic Reassignment of Staphylococcus schleiferi Subspecies into Two Separate Species, Staphylococcus schleiferi and Staphylococcus coagulans. Microbiol. Spectr. 2023, 11, e0467022. [Google Scholar] [CrossRef]
- Madhaiyan, M.; Wirth, J.S.; Saravanan, V.S. Phylogenomic analyses of the Staphylococcaceae family suggest the reclassification of five species within the genus Staphylococcus as heterotypic synonyms, the promotion of five subspecies to novel species, the taxonomic reassignment of five Staphylococcus species to Mammaliicoccus gen. nov., and the formal assignment of Nosocomiicoccus to the family Staphylococcaceae. Int. J. Syst. Evol. Microbiol. 2020, 70, 5926–5936. [Google Scholar]
- Ashelford, K.E.; Chuzhanova, N.A.; Fry, J.C.; Jones, A.J.; Weightman, A.J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 2005, 71, 7724–7736. [Google Scholar] [CrossRef]
- Vandenesch, F.; Lebeau, C.; Bes, M.; Lina, G.; Lina, B.; Greenland, T.; Benito, Y.; Brun, Y.; Fleurette, J.; Etienne, J. Clotting activity in Staphylococcus schleiferi subspecies from human patients. J. Clin. Microbiol. 1994, 32, 388–392. [Google Scholar] [CrossRef]
- Lefort, V.; Desper, R.; Gascuel, O. FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program. Mol. Biol. Evol. 2015, 32, 2798–2800. [Google Scholar] [CrossRef]
- Abouelkhair, M.A.; Rifkin, R.E.; Grzeskowiak, R.M.; Biris, A.S.; Anderson, D.E.; Bemis, D.A.; Kania, S.A. Complete Genome Sequences of Four Staphylococcus aureus Sequence Type 398 Isolates from Four Goats with Osteomyelitis. Microbiol. Resour. Announc. 2018, 6, e01599-17. [Google Scholar] [CrossRef]
- Billings, C.; Rifkin, R.; Abouelkhair, M.; Jones, R.D.; Bow, A.; Kolape, J.; Rajeev, S.; Kania, S.; Anderson, D.E. In vitro and in vivo assessment of caprine origin Staphylococcus aureus ST398 strain UTCVM1 as an osteomyelitis pathogen. Front. Cell Infect Microbiol. 2022, 12, 1015655. [Google Scholar] [CrossRef]
- Abebe, A.A.; Birhanu, A.G. Methicillin Resistant Staphylococcus aureus: Molecular Mechanisms Underlying Drug Resistance Development and Novel Strategies to Combat. Infect Drug Resist 2023, 16, 7641–7662. [Google Scholar] [CrossRef]
- Aung, M.S.; Urushibara, N.; Kawaguchiya, M.; Ohashi, N.; Hirose, M.; Kimura, Y.; Kudo, K.; Ito, M.; Kobayashi, N. Molecular Epidemiological Characterization of Methicillin-Resistant Staphylococcus aureus from Bloodstream Infections in Northern Japan: Increasing Trend of CC1 and Identification of ST8-SCCmec IVa USA300-Like Isolate Lacking Arginine Catabolic Mobile Element. Microb. Drug Resist 2023, 30, 63–72. [Google Scholar]
- Kim, Y.H.; Park, J.; Chung, H.S. Genetic characterization of tetracycline-resistant Staphylococcus aureus with reduced vancomycin susceptibility using whole-genome sequencing. Arch. Microbiol. 2023, 206, 24. [Google Scholar] [CrossRef]
- Ko, D.S.; Kim, N.H.; Kim, E.K.; Ha, E.J.; Ro, Y.H.; Kim, D.; Choi, K.S.; Kwon, H.J. Comparative genomics of bovine mastitis-origin Staphylococcus aureus strains classified into prevalent human genotypes. Res. Vet. Sci. 2021, 139, 67–77. [Google Scholar] [CrossRef]
- Makarova, O.; Johnston, P.; Rodriguez-Rojas, A.; El Shazely, B.; Morales, J.M.; Rolff, J. Genomics of experimental adaptation of Staphylococcus aureus to a natural combination of insect antimicrobial peptides. Sci. Rep. 2018, 8, 15359. [Google Scholar] [CrossRef]
- Abouelkhair, M.A.; Bemis, D.A.; Giannone, R.J.; Frank, L.A.; Kania, S.A. Identification, cloning and characterization of SpEX exotoxin produced by Staphylococcus pseudintermedius. PLoS ONE 2019, 14, e0220301. [Google Scholar] [CrossRef]
- Abouelkhair, M.A.; Frank, L.A.; Bemis, D.A.; Giannone, R.J.; Kania, S.A. Staphylococcus pseudintermedius 5’-nucleotidase suppresses canine phagocytic activity. Vet. Microbiol. 2020, 246, 108720. [Google Scholar] [CrossRef]
- Abouelkhair, M.A.; Thompson, R.; Riley, M.C.; Bemis, D.A.; Kania, S.A. Complete Genome Sequences of Three Staphylococcus pseudintermedius Strains Isolated from Botswana. Genome Announc. 2018, 6, 10-128. [Google Scholar] [CrossRef]
- Phophi, L.; Abouelkhair, M.; Jones, R.; Henton, M.; Qekwana, D.N.; Kania, S.A. The molecular epidemiology and antimicrobial resistance of Staphylococcus pseudintermedius canine clinical isolates submitted to a veterinary diagnostic laboratory in South Africa. PLoS ONE 2023, 18, e0290645. [Google Scholar] [CrossRef]
- Griffeth, G.C.; Morris, D.O.; Abraham, J.L.; Shofer, F.S.; Rankin, S.C. Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet. Dermatol. 2008, 19, 142–149. [Google Scholar] [CrossRef]
- Huse, H.K.; Miller, S.A.; Chandrasekaran, S.; Hindler, J.A.; Lawhon, S.D.; Bemis, D.A.; Westblade, L.F.; Humphries, R.M. Evaluation of Oxacillin and Cefoxitin Disk Diffusion and MIC Breakpoints Established by the Clinical and Laboratory Standards Institute for Detection of mecA-Mediated Oxacillin Resistance in Staphylococcus schleiferi. J. Clin. Microbiol. 2018, 56, e01653-17. [Google Scholar] [CrossRef]
- Roberts, S.; O’Shea, K.; Morris, D.; Robb, A.; Morrison, D.; Rankin, S. A real-time PCR assay to detect the Panton Valentine Leukocidin toxin in staphylococci: Screening Staphylococcus schleiferi subspecies coagulans strains from companion animals. Vet. Microbiol. 2005, 107, 139–144. [Google Scholar] [CrossRef]
- Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28, 1647–1649. [Google Scholar] [CrossRef]
- Gurevich, A.; Saveliev, V.; Vyahhi, N.; Tesler, G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 2013, 29, 1072–1075. [Google Scholar] [CrossRef]
- Meier-Kolthoff, J.P.; Goker, M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat. Commun. 2019, 10, 2182. [Google Scholar] [CrossRef]
- Meier-Kolthoff, J.P.; Carbasse, J.S.; Peinado-Olarte, R.L.; Goker, M. TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic. Acids Res. 2022, 50, D801–D807. [Google Scholar] [CrossRef]
- Ondov, B.D.; Treangen, T.J.; Melsted, P.; Mallonee, A.B.; Bergman, N.H.; Koren, S.; Phillippy, A.M. Mash: Fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016, 17, 132. [Google Scholar] [CrossRef]
- Lagesen, K.; Hallin, P.; Rodland, E.A.; Staerfeldt, H.H.; Rognes, T.; Ussery, D.W. RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007, 35, 3100–3108. [Google Scholar] [CrossRef]
- Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009, 10, 421. [Google Scholar] [CrossRef]
- Meier-Kolthoff, J.P.; Auch, A.F.; Klenk, H.P.; Goker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 2013, 14, 60. [Google Scholar] [CrossRef]
- Farris, J.S. Estimating Phylogenetic Trees from Distance Matrices. Am. Nat. 1972, 106, 645–668. [Google Scholar] [CrossRef]
- Kreft, L.; Botzki, A.; Coppens, F.; Vandepoele, K.; Van Bel, M. PhyD3: A phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 2017, 33, 2946–2947. [Google Scholar] [CrossRef]
- Meier-Kolthoff, J.P.; Hahnke, R.L.; Petersen, J.; Scheuner, C.; Michael, V.; Fiebig, A.; Rohde, C.; Rohde, M.; Fartmann, B.; Goodwin, L.A.; et al. Complete genome sequence of DSM 30083(T), the type strain (U5/41(T)) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand. Genomic Sci. 2014, 9, 2. [Google Scholar] [CrossRef]
- Eren, A.M.; Kiefl, E.; Shaiber, A.; Veseli, I.; Miller, S.E.; Schechter, M.S.; Fink, I.; Pan, J.N.; Yousef, M.; Fogarty, E.C.; et al. Community-led, integrated, reproducible multi-omics with anvi’o. Nat. Microbiol. 2021, 6, 3–6. [Google Scholar] [CrossRef]
- Pritchard, L.; Glover, R.H.; Humphris, S.; Elphinstone, J.G.; Toth, I.K. Genomics and taxonomy in diagnostics for food security: Soft-rotting enterobacterial plant pathogens. Anal. Methods 2016, 8, 12–24. [Google Scholar] [CrossRef]
- Pritchard, L.; Harrington, B.; Cock, P.; Davey, R.; Waters, N.; Sharma, A.; Balázs Brankovics, Y.T.; Esen, Ö. widdowquinn/pyani: Application and Python Module. 2022. Available online: https://zenodo.org/record/6927794 (accessed on 20 December 2023).
- Lee, I.; Ouk Kim, Y.; Park, S.-C.; Chun, J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 2016, 66, 1100–1103. [Google Scholar] [CrossRef]
- Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 2014, 30, 2068–2069. [Google Scholar] [CrossRef]
- Page, A.J.; Cummins, C.A.; Hunt, M.; Wong, V.K.; Reuter, S.; Holden, M.T.G.; Fookes, M.; Falush, D.; Keane, J.A.; Parkhill, J. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015, 31, 3691–3693. [Google Scholar] [CrossRef]
- Kaas, R.S.; Leekitcharoenphon, P.; Aarestrup, F.M.; Lund, O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS ONE 2014, 9, e104984. [Google Scholar] [CrossRef]
- Hammond, A.J.; Binsker, U.; Aggarwal, S.D.; Ortigoza, M.B.; Loomis, C.; Weiser, J.N. Neuraminidase B controls neuraminidase A-dependent mucus production and evasion. PLoS Pathog. 2021, 17, e1009158. [Google Scholar] [CrossRef]
- Osman, D.; Piergentili, C.; Chen, J.; Sayer, L.N.; Uson, I.; Huggins, T.G.; Robinson, N.J.; Pohl, E. The Effectors and Sensory Sites of Formaldehyde-responsive Regulator FrmR and Metal-sensing Variant. J. Biol. Chem. 2016, 291, 19502–19516. [Google Scholar] [CrossRef]
- Heilbronner, S.; Holden, M.T.; van Tonder, A.; Geoghegan, J.A.; Foster, T.J.; Parkhill, J.; Bentley, S.D. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 2011, 322, 60–67. [Google Scholar] [CrossRef]
- Jamdar, S.N.; Are, V.N.; Navamani, M.; Kumar, S.; Nagar, V.; Makde, R.D. The members of M20D peptidase subfamily from Burkholderia cepacia, Deinococcus radiodurans and Staphylococcus aureus (HmrA) are carboxydipeptidases, primarily specific for Met-X dipeptides. Arch Biochem. Biophys. 2015, 587, 18–30. [Google Scholar] [CrossRef]
- Singh, V.; Phukan, U.J. Interaction of host and Staphylococcus aureus protease-system regulates virulence and pathogenicity. Med. Microbiol. Immunol. 2019, 208, 585–607. [Google Scholar] [CrossRef]
- Bradley, N.P.; Washburn, L.A.; Christov, P.P.; Watanabe, C.M.H.; Eichman, B.F. Escherichia coli YcaQ is a DNA glycosylase that unhooks DNA interstrand crosslinks. Nucleic Acids Res. 2020, 48, 7005–7017. [Google Scholar]
- Jimenez-Mejia, R.; Campos-Garcia, J.; Cervantes, C. Membrane topology of the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 2006, 262, 178–184. [Google Scholar] [CrossRef]
- Soto, S.M. Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence 2013, 4, 223–229. [Google Scholar] [CrossRef]
Isolate | GenBank Accession Number |
---|---|
S. schleferi MGYG-HGUT-01437 | GCA_902374935.1 |
S. coagulans 2317-03 | GCA_001188915.1 |
S. coagulans OT1-1 | GCA_004026205.1 |
S. coagulans 5909-02 | GCA_001188875.1 |
S. coagulans TSCC54 | GCA_001548255.1 |
S. coagulans reference genome | GCA_022557135.1 |
S. coagulans 2142-05 | GCA_001188895.1 |
Strain | WGS Accession No * | No of Contigs | N50 (bp) | Genome Length (bp) | G+C Content (%) | Predicted Coding Sequences | Predicted RNAs |
---|---|---|---|---|---|---|---|
Staphylococcus coagulans 191 | PNRJ00000000 | 51 | 138,893 | 2,508,133 | 35.73 | 2294 | 72 |
Staphylococcus schleiferi 192 | POVG00000000 | 102 | 59,786 | 2,452,487 | 35.87 | 2203 | 74 |
Staphylococcus coagulans 196 | POVH00000000 | 56 | 110,279 | 2,508,604 | 35.74 | 2299 | 74 |
Staphylococcus schleiferi 205 | POVI00000000 | 92 | 56,958 | 2,468,342 | 35.92 | 2218 | 76 |
Staphylococcus schleiferi 214 | POVJ00000000 | 94 | 57,247 | 2,469,699 | 35.92 | 2216 | 76 |
Staphylococcus schleiferi ATCC 43808T | POVK00000000 | 88 | 56,938 | 2,469,638 | 35.92 | 2218 | 73 |
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Abouelkhair, M.A.; Kania, S.A. Whole Genome Sequencing and Comparative Genomics of Six Staphylococcus schleiferi and Staphylococcus coagulans Isolates. Genes 2024, 15, 284. https://doi.org/10.3390/genes15030284
Abouelkhair MA, Kania SA. Whole Genome Sequencing and Comparative Genomics of Six Staphylococcus schleiferi and Staphylococcus coagulans Isolates. Genes. 2024; 15(3):284. https://doi.org/10.3390/genes15030284
Chicago/Turabian StyleAbouelkhair, Mohamed A., and Stephen A. Kania. 2024. "Whole Genome Sequencing and Comparative Genomics of Six Staphylococcus schleiferi and Staphylococcus coagulans Isolates" Genes 15, no. 3: 284. https://doi.org/10.3390/genes15030284
APA StyleAbouelkhair, M. A., & Kania, S. A. (2024). Whole Genome Sequencing and Comparative Genomics of Six Staphylococcus schleiferi and Staphylococcus coagulans Isolates. Genes, 15(3), 284. https://doi.org/10.3390/genes15030284