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. 2019 Apr 25;8(17):e00062-19. doi: 10.1128/MRA.00062-19

Draft Genome Sequences of 64 Type Strains of 50 Species and 25 Subspecies of the Genus Staphylococcus Rosenbach 1884

Kevin Cole a,b,c,, Dona Foster d, Julie E Russell f, Tanya Golubchik d,e, Martin Llewelyn b,c, Daniel J Wilson d,g, Derrick Crook a,d, John Paul, Modernising Medical Microbiology Consortiuma,b
Editor: Jason E Stajichh
PMCID: PMC6486237  PMID: 31023808

Members of the genus Staphylococcus have been isolated from humans, animals, and the environment. Accurate identification with whole-genome sequencing requires access to data derived from type strains.

ABSTRACT

Members of the genus Staphylococcus have been isolated from humans, animals, and the environment. Accurate identification with whole-genome sequencing requires access to data derived from type strains. We provide sequence data for type strains of 64 taxa in the genus that at the time of this writing have standing in the nomenclature.

ANNOUNCEMENT

The term “Staphylococcus” was introduced by Sir Alexander Ogston in reference to the bunch-of-grapes-like appearance that distinguishes these organisms from streptococci (1). Friedrich Rosenbach subsequently described “Staphylococcus pyogenes aureus” and “Staphylococcus pyogenes albus” (2). At the time of this writing, the genus includes 51 species plus additional subspecies. They are nonmotile, facultatively or obligatory anaerobic, Gram-positive cocci (35). Most are catalase positive (46). Members of the genus include human and animal pathogens and commensals, and they have been isolated from foodstuffs and environmental sources (7, 8). S. aureus is a well-known human pathogen, and the genome sequence of the type strain was published by Kim et al. in 2014 (9) and Shiroma et al. in 2015 (10). Other staphylococci are increasingly becoming recognized as clinically important (7, 11) and are being investigated accordingly (12, 13).

Here we give information for genome sequences of 64 type strains (Table 1) representing 50 species in the genus Staphylococcus that have standing in the nomenclature at the time of writing plus a number of subspecies. This catalogue of sequences can be employed as a resource for taxonomic study and to identify test isolates.

TABLE 1.

Accessions and genomic characteristics of 64 type strains of the genus Staphylococcus Rosenbach 1884

Species Strain No. of total reads No. of contigs Contig N50 value (bp) G+C content (%) Depth (×) Length (bp) No. of genes
Staphylococcus agnetis Taponen et al. 2012 DSM 23656 1,978,702 164 38,640 34.6 66.4 2,491,359 2,514
Staphylococcus argensis Heß and Gallert 2015 DSM 29875 1,430,626 19 98,914 40.8 24.75 2,452,468 2,350
Staphylococcus argenteus Tong et al. 2015 DSM 28299 1,686,623 48 96,207 35.1 31.51 2,759,629 2,741
Staphylococcus arlettae Schleifer et al. 1985 NCTC 12413 1,992,335 33 66,907 36.2 26.57 2,665,344 2,600
Staphylococcus aureus subsp. anaerobius De La Fuente et al. 1985 DSM 20714 1,949,112 400 14,564 33.2 56.12 2,575,746 2,738
Staphylococcus aureus subsp. aureus De La Fuente et al. 1985 NCTC 08532 2,207,024 41 66,458 34.9 32.75 2,749,019 2,887
Staphylococcus auricularis Kloos and Schleifer 1983 NCTC 12101 1,517,960 103 39,462 37.6 38.94 2,201,622 2,416
Staphylococcus capitis subsp. capitis Bannerman and Kloos 1991 NCTC 11045 2,331,749 51 101,914 36 38.76 2,434,909 2,419
Staphylococcus capitis subsp. urealyticus Bannerman and Kloos 1991 DSM 6717 1,467,277 184 42,481 35.7 35.79 2,468,245 2,500
Staphylococcus caprae Devriese et al. 1983 NCTC 12196 2,647,473 101 62,212 33.6 62.25 2,606,761 2,551
Staphylococcus carnosus subsp. carnosus Probst et al. 1998 DSM 20501 1,442,326 70 247,399 37.7 90.42 2,434,039 2,447
Staphylococcus carnosus subsp. utilis Probst et al. 1998 DSM 11676 1,834,824 444 11,755 33.4 36.49 2,622,255 2,702
Macrococcus caseolyticus Schleifer et al. 1982 DSM 20597 1,614,157 122 46,917 35.5 70.8 2,171,833 2,341
Staphylococcus chromogenes Hájek et al. 1987 NCTC 10530 1,169,641 117 55,359 38.5 35.94 2,276,768 2,265
Staphylococcus cohnii subsp. cohnii Kloos and Wolfshohl 1991 NCTC 11041 1,727,741 69 107,943 34.9 26.83 2,637,875 2,588
Staphylococcus cohnii subsp. urealyticus Kloos and Wolfshohl 1991 DSM 6718 1,780,154 189 26,500 33.8 49.2 2,670,427 2,647
Staphylococcus condimenti Probst et al. 1998 DSM 11674 1,493,311 211 32,221 35.8 23.6 2,615,688 2,604
Staphylococcus delphini Varaldo et al. 1988 NCTC 12225 1,499,070 227 42,122 37.1 52.47 2,751,077 2,716
Staphylococcus devriesei Supré et al. 2010 CCUG 58238 2,004,126 129 49,574 35.6 44.18 2,379,883 2,392
Staphylococcus epidermidis Kloos and Schleifer 1975 NCTC 11047 1,852,043 62 55,347 35.8 38.72 2,442,385 2,438
Staphylococcus equorum subsp. equorum Place et al. 2003 NCTC 12414 1,523,028 93 44,027 33.2 87.8 2,350,071 2,590
Staphylococcus equorum subsp. linens Place et al. 2003 DSM 15097 1,911,830 101 55,558 34 45.91 2,768,268 2,739
Staphylococcus felis Igimi et al. 1989 DSM 7377 1,572,866 244 24,395 36.1 45 2,409,047 2,389
Staphylococcus fleurettii Vernozy-Rozand et al. 2000 DSM 13212 1,811,506 156 38,940 31.7 90.36 2,473,007 2,489
Staphylococcus haemolyticus Kloos and Schleifer 1975 NCTC 11042 1,975,151 92 55,720 36 35.24 2,472,399 2,466
Staphylococcus hominis subsp. hominis Kloos et al. 1998 NCTC 11320 2,793,372 30 144,174 39.1 47.59 2,204,528 2,214
Staphylococcus hominis subsp. novobiosepticus Kloos et al. 1998 CCUG 42399 2,349,019 166 35,627 33.4 54.32 2,422,390 2,498
Staphylococcus hyicus Hájek et al. 1987 CCUG 6509 2,111,770 134 37,537 37.7 91.88 2,633,558 2,222
Staphylococcus intermedius Hájek 1976 NCTC 11048 2,212,778 176 51,566 37.8 41.45 2,801,199 2,797
Staphylococcus kloosii Schleifer et al. 1985 NCTC 12415 2,000,256 134 36,209 33 74.73 2,607,914 2,642
Staphylococcus lentus Schleifer et al. 1983 NCTC 12102 3,158,427 79 86,117 32.7 93.32 2,546,437 2,579
Staphylococcus lugdunensis Freney et al. 1988 NCTC 12217 2,272,326 20 94,638 39.8 35.15 2,519,514 2,409
Staphylococcus lutrae Foster et al. 1997 DSM 10244 1,461,603 200 41,148 37.8 42.6 2,429,515 2,354
Staphylococcus massiliensis Al Masalma et al. 2010 CCUG 55927 2,070,218 212 32,379 35 41.69 2,348,540 2,305
Staphylococcus microti Nováková et al. 2010 DSM 22147 1,582,916 191 38,659 39.1 53.13 2,409,945 2,429
Staphylococcus muscae Hájek et al. 1992 DSM 7068 1,986,642 183 32,200 37.4 63.32 2,049,263 2,075
Staphylococcus nepalensis Spergser et al. 2003 DSM 15150 2,186,623 412 13,339 32.9 50.09 2,860,226 2,790
Staphylococcus pasteuri Chesneau et al. 1993 DSM 10656 1,952,357 233 25,197 31.4 89.61 2,605,275 2,277
Staphylococcus petrasii subsp. croceilyticus Pantůček et al. 2013 CCUG 62728 1,665,214 147 36,044 34.6 55.76 2,380,571 2,346
Staphylococcus petrasii subsp. jettensis De Bel et al. 2014 CCUG 62657 1,923,933 266 23,568 34.7 45.4 2,709,801 2,730
Staphylococcus petrasii subsp. petrasii Pantůček et al. 2013 CCUG 62727 2,674,384 139 46,072 34.1 58.57 2,486,611 2,508
Staphylococcus petrasii subsp. pragensis Švec et al. 2015 DSM 102853 2,071,432 493 11,863 33 87.81 3,094,570 3,040
Staphylococcus pettenkoferi Trülzsch et al. 2007 CCUG 51270 1,933,064 122 62,580 37.2 46.82 2,455,272 2,399
Staphylococcus piscifermentans Tanasupawat et al. 1992 DSM 7373 1,828,752 147 37,718 37 91.44 2,711,458 2,470
Staphylococcus pseudintermedius Devriese et al. 2005 CCUG 49543 1,307,526 245 32,222 37.3 33.7 2,507,403 2,482
Staphylococcus pulvereri Zakrzewska-Czerwińska et al. 1995 DSM 9930 1,085,309 252 21,767 32.8 91.9 2,507,841 2,321
Staphylococcus rostri Riesen and Perreten 2010 DSM 21968 1,857,275 167 39,749 37.6 72.78 2,341,022 2,342
Staphylococcus saccharolyticus Kilpper-Bälz and Schleifer 1984 NCTC 11807 1,735,439 93 46,092 34.5 91.58 2,462,952 2,724
Staphylococcus saprophyticus subsp. bovis Hájek et al. 1996 CCUG 38042 1,774,718 289 16,602 32.9 48.26 2,709,959 2,757
Staphylococcus saprophyticus subsp. saprophyticus Hájek et al. 1996 NCTC 7292 2,626,126 123 46,677 33.3 90.52 2,589,171 2,567
Staphylococcus schleiferi subsp. coagulans Igimi et al. 1990 DSM 6628 1,893,687 155 54,157 36.2 41.27 2,443,567 2,378
Staphylococcus schleiferi subsp. schleiferi Igimi et al. 1990 NCTC 12218 3,174,090 98 67,466 37.6 90.54 2,896,454 2,368
Staphylococcus schweitzeri Tong et al. 2015 DSM 28300 1,956,713 52 65,148 35.5 37.08 2,743,713 2,725
Staphylococcus sciuri subsp. carnaticus Kloos et al. 1997 CCUG 39509 1,454,961 182 40,393 33.6 51.84 2,877,673 2,983
Staphylococcus sciuri subsp. rodentium Kloos et al. 1997 CCUG 37923 925,469 82 62,754 36.6 91.96 2,449,200 2,919
Staphylococcus sciuri subsp. sciuri Kloos et al. 1997 NCTC 12103 2,205,792 37 123,278 38.7 32.97 2,768,322 2,760
Staphylococcus simiae Pantucek et al. 2005 CCUG 51256 2,569,797 159 45,657 34.3 77.79 2,598,081 2,523
Staphylococcus simulans Kloos and Schleifer 1975 NCTC 11046 1,359,349 99 84,647 37.2 48.33 2,735,408 2,699
Staphylococcus stepanovicii Hauschild et al. 2012 DSM 26319 1,676,662 140 42,374 35.1 36.62 2,406,018 2,468
Staphylococcus succinus subsp. casei Place et al. 2003 DSM 15096 1,816,917 169 29,746 34.8 56.18 2,871,374 2,802
Staphylococcus succinus subsp. succinus Place et al. 2003 DSM 14617 1,805,866 339 18,694 32.2 29.39 2,786,115 2,764
Staphylococcus vitulinus Webster et al. 1994 DSM 15615 1,414,448 259 23,873 32.5 57.23 2,595,808 2,674
Staphylococcus warneri Kloos and Schleifer 1975 NCTC 11044 1,997,389 31 115,611 38 35.2 2,401,190 2,353
Staphylococcus xylosus Schleifer and Kloos 1975 NCTC 11043 1,802,579 226 25,849 34.4 51.79 2,725,582 2,615

Organisms were obtained from the National Collection of Type Cultures, United Kingdom (NCTC), Deutsche Sammlung von Mikroorganismen und Zellkulturen, Germany (DSMZ), and Culture Collection, University of Göteborg, Sweden (CCUG).

Isolates were cultured on a Columbia agar and horse blood (CBA) plate (Oxoid Ltd., Basingstoke, UK) and incubated aerobically or anaerobically at 35°C overnight. Bacterial biomass was scraped from cultured plates for DNA extraction. DNA was extracted and purified with a QuickGene DNA tissue kit (AutoGen, Holliston, MA, USA). Extracted DNA was prepared for sequencing following NexteraXT (Illumina, San Diego, CA, USA) protocols and sequenced as 150-bp paired-end reads on the Illumina MiSeq platform. Reads were stripped of adaptors with BBDuk 34.38 (14). Illumina reads were quality controlled by calling bases only when 5 or more were present at a position and supported by at least 1 high-quality read in forward and reverse directions. Reads were assembled using Velvet 1.2.10 (15) with kmer size and coverage estimated with VelvetOptimiser 2.1.7 (15). To ensure assembly quality, at least 97% of the total assembly was required to be in contigs larger than 1 kb. Draft genome sequences were annotated with Prokka 1.12 (16).

Genome sizes varied between 2.1 million and 3.1 million base pairs across the genus, with G+C contents ranging from 31.4% to 40.8%. The genome sequences contained a range of 2,075 to 3,040 annotated genes.

Data availability.

All sequences discussed here have been deposited in GenBank as BioProject number PRJNA339206. Table 1 lists individual accession numbers by taxon. These Sequence Read Archive deposits can be found under the study number SRP093495.

ACKNOWLEDGMENTS

We thank Ana Deheer-Graham, NCTC, Public Health England, United Kingdom, for help in obtaining isolates; Nick Sanderson, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom, for helping with the analysis pipeline; and Ian Szwajca, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom, for uploading genome sequences to GenBank.

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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

All sequences discussed here have been deposited in GenBank as BioProject number PRJNA339206. Table 1 lists individual accession numbers by taxon. These Sequence Read Archive deposits can be found under the study number SRP093495.


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