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 (3–5). Most are catalase positive (4–6). 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.