Staphylococcus edaphicus sp. nov., isolated in Antarctica, harbors the mecC gene and genomic islands with a suspected role in adaptation to extreme environments

Applied and Environmental Microbiology

Volumn 84, Issue 2, 2018, Pages

  Pantüček, Roman ^a   Sedláček, Ivo ^a   Indráková, Adéla ^a   Vrbovská, Veronika ^a   Mašlaňová, Ivana ^a   Kovařovic, Vojtěch ^a   Švec, Pavel ^a   Králová, Stanislava ^a   Krištofová, Lucie ^a   Kekláková, Jana ^b   Petráš, Petr ^b   Doškař, Jiří ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

^b NATIONAL INSTITUTE OF PUBLIC HEALTH   (Czech Republic)

Author keywords

Beta lactams; Chromosomal islands; Coagulase negative staphylococci; Drug resistance evolution; Genomics; Methicillin resistance; Mobile genetic elements; Pathogenicity islands; Penicillin binding proteins; Phylogenetic analysis; Polyphasic taxonomy

Indexed keywords

ANTIBIOTICS; CHROMOSOMES; DNA; DRUG PRODUCTS; DRUG THERAPY; MASS SPECTROMETRY; PLANTS (BOTANY); POLYACRYLATES; RNA;

BETA-LACTAMS; CHROMOSOMAL ISLANDS; COAGULASE-NEGATIVE STAPHYLOCOCCI; DRUG RESISTANCE; GENETIC ELEMENTS; GENOMICS; METHICILLIN; PATHOGENICITY ISLANDS; PENICILLIN- BINDING PROTEINS; PHYLOGENETIC ANALYSIS; POLYPHASIC;

GENES;

ANTIBIOTIC RESISTANCE; BACTERIUM; CHEMICAL BINDING; CHROMOSOME; DISEASE RESISTANCE; GENOME; HYBRIDIZATION; MICROBIAL ECOLOGY; NEW SPECIES; PATHOGENICITY; PHYLOGENETICS; POLAR REGION; RNA; SANDY SOIL; TAXONOMY;

ANTARCTICA; JAMES ROSS ISLAND; WEST ANTARCTICA;

STAPHYLOCOCCUS; STAPHYLOCOCCUS SAPROPHYTICUS; STAPHYLOCOCCUS SAPROPHYTICUS SUBSP. SAPROPHYTICUS;

ADAPTATION; ANTARCTICA; BACTERIAL GENE; CLASSIFICATION; COLD; EXTREME ENVIRONMENT; GENETICS; GENOMIC ISLAND; PHYSIOLOGY; STAPHYLOCOCCUS;

ADAPTATION, BIOLOGICAL; ANTARCTIC REGIONS; EXTREME COLD; EXTREME ENVIRONMENTS; GENES, BACTERIAL; GENOMIC ISLANDS; STAPHYLOCOCCUS;

EID: 85039855848     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01746-17     Document Type: Article

References (75)

1. Götz F, Bannerman T, Schleifer K-H. 2006. The genera Staphylococcus and Macrococcus, p 5-75. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The Prokaryotes: Bacteria, Firmicutes, Cyanobacteria, vol 4. Springer US, New York, NY. https://doi.org/10.1007/0-387-30744-3_1
2. Emmett M, Kloos WE. 1975. Amino acid requirements of staphylococci isolated from human skin. Can J Microbiol 21:729-733. https://doi.org/10.1139/m75-107
3. Emmett M, Kloos WE. 1979. The nature of arginine auxotrophy in cutaneous populations of staphylococci. J Gen Microbiol 110:305-314. https://doi.org/10.1099/00221287-110-2-305
4. Lambert LH, Cox T, Mitchell K, Rossello-Mora RA, Del Cueto C, Dodge DE, Orkand P, Cano RJ. 1998. Staphylococcus succinus sp. nov., isolated from Dominican amber. Int J Syst Bacteriol 48:511-518. https://doi.org/10.1099/00207713-48-2-511
5. Hess S, Gallert C. 2015. Staphylococcus argensis sp nov., a hovel staphylococcal species isolated from an aquatic environment. Int J Syst Evol Microbiol 65:2661-2665. https://doi.org/10.1099/ijs.0.000319
6. Kloos WE. 1980. Natural populations of the genus Staphylococcus. Annu Rev Microbiol 34:559-592. https://doi.org/10.1146/annurev.mi.34.100180.003015
7. Kloos WE, Schleifer KH, Smith RF. 1976. Characterization of Staphylococcus sciuri sp. nov. and its subspecies. Int J Syst Bacteriol 26:22-37. https://doi.org/10.1099/00207713-26-1-22
8. Planchon S, Gaillard-Martinie B, Dordet-Frisoni E, Bellon-Fontaine MN, Leroy S, Labadie J, Hebraud M, Talon R. 2006. Formation of biofilm by Staphylococcus xylosus. Int J Food Microbiol 109:88-96. https://doi.org/10.1016/j.ijfoodmicro.2006.01.016
9. Dordet-Frisoni E, Dorchies G, De Araujo C, Talon R, Leroy S. 2007. Genomic diversity in Staphylococcus xylosus. Appl Environ Microbiol 73:7199-7209. https://doi.org/10.1128/AEM.01629-07
10. Irlinger F. 2008. Safety assessment of dairy microorganisms: coagulasenegative staphylococci. Int J Food Microbiol 126:302-310. https://doi.org/10.1016/j.ijfoodmicro.2007.08.016
11. Giordano N, Corallo C, Miracco C, Papakostas P, Montella A, Figura N, Nuti R. 2016. Erythema nodosum associated with Staphylococcus xylosus septicemia. J Microbiol Immunol Infect 49:134-137. https://doi.org/10.1016/j.jmii.2012.10.003
12. Becker K, von Eiff C. 2011. Staphylococcus, Micrococcus, and other catalase-positive cocci, p 308-330. In Versalovic J, Carroll KC, Funke G, Jorgensen JH, Landry ML, Warnock DW (ed), Manual of clinical microbiology, 10th ed. ASM Press, Washington, DC. https://doi.org/10.1128/9781555816728.ch19
13. Schleifer KH, Kloos WE. 1975. Isolation and characterization of staphylococci from human skin. 1. Amended descriptions of Staphylococcus epidermidis and Staphylococcus saprophyticus and descriptions of 3 new species-Staphylococcus cohnii, Staphylococcus haemolyticus, and Staphylococcus xylosus. Int J Syst Bacteriol 25:50-61. https://doi.org/10.1099/00207713-25-1-50
14. Widerström M, Wiström J, Sjöstedt A, Monsen T. 2012. Coagulasenegative staphylococci: update on the molecular epidemiology and clinical presentation, with a focus on Staphylococcus epidermidis and Staphylococcus saprophyticus. Eur J Clin Microbiol Infect Dis 31:7-20. https://doi.org/10.1007/s10096-011-1270-6
15. Takahashi T, Satoh I, Kikuchi N. 1999. Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis. Int J Syst Bacteriol 49:725-728. https://doi.org/10.1099/00207713-49-2-725
16. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morikawa K, Higashide M, Maruyama A, Inose Y, Matoba K, Toh H, Kuhara S, Hattori M, Ohta T. 2005 Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. Proc Natl Acad Sci U S A 102:13272-13277. https://doi.org/10.1073/pnas.0502950102
17. Schleifer K-H, Bell JA. 2009. Genus I. Staphylococcus Rosenbach 1884, 18AL (Nom. Cons. Opin 17 Jud. Comm. 1958, 153.), p 392-421. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (ed), Bergey's manual of systematic bacteriology, vol 3. The Firmicutes. Springer-Verlag, New York, NY. https://doi.org/10.1007/978-0-387-68489-5
18. Foster TJ, Geoghegan JA, Ganesh VK, Hook M. 2014. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12:49-62. https://doi.org/10.1038/nrmicro3161
19. Wilson LK, Coombs GW, Christiansen K, Grubb WB, O'Brien FG. 2016. Characterization of a novel staphylococcal cassette chromosome composite island from community-associated MRSA isolated in aged care facilities in Western Australia. J Antimicrob Chemother 71:3372-3375. https://doi.org/10.1093/jac/dkw317
20. Ohniwa RL, Kitabayashi K, Morikawa K. 2013. Alternative cardiolipin synthase Cls1 compensates for stalled Cls2 function in Staphylococcus aureus under conditions of acute acid stress. FEMS Microbiol Lett 338: 141-146. https://doi.org/10.1111/1574-6968.12037
21. Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, Saito S, Hayashi H, Morikawa K. 2011. Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. BMC Microbiol 11:13. https://doi.org/10.1186/1471-2180-11-13
22. Peleg AY, Miyakis S, Ward DV, Earl AM, Rubio A, Cameron DR, Pillai S, Moellering RC, Jr, Eliopoulos GM. 2012. Whole genome characterization of the mechanisms of daptomycin resistance in clinical and laboratory derived isolates of Staphylococcus aureus. PLoS One 7:e28316. https://doi.org/10.1371/journal.pone.0028316
23. International Working Group on the Classification of Staphylococcal Cassette Chromosome E. 2009. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961-4967. https://doi.org/10.1128/AAC.00579-09
24. García-álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA. 2011. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11: 595-603. https://doi.org/10.1016/S1473-3099(11)70126-8
25. Harrison EM, Paterson GK, Holden MT, Morgan FJ, Larsen AR, Petersen A, Leroy S, De Vliegher S, Perreten V, Fox LK, Lam TJ, Sampimon OC, Zadoks RN, Peacock SJ, Parkhill J, Holmes MA. 2013. A Staphylococcus xylosus isolate with a new mecC allotype. Antimicrob Agents Chemother 57: 1524-1528. https://doi.org/10.1128/AAC.01882-12
26. Malyszko I, Schwarz S, Hauschild T. 2014. Detection of a new mecC allotype, mecC2, in methicillin-resistant Staphylococcus saprophyticus. J Antimicrob Chemother 69:2003-2005. https://doi.org/10.1093/jac/dku043
27. Paterson GK, Larsen AR, Robb A, Edwards GE, Pennycott TW, Foster G, Mot D, Hermans K, Baert K, Peacock SJ, Parkhill J, Zadoks RN, Holmes MA. 2012 The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother 67:2809-2813. https://doi.org/10.1093/jac/dks329
28. Monecke S, Gavier-Widen D, Mattsson R, Rangstrup-Christensen L, Lazaris A, Coleman DC, Shore AC, Ehricht R. 2013. Detection of mecC-positive Staphylococcus aureus (CC130-MRSA-XI) in diseased European hedgehogs (Erinaceus europaeus) in Sweden. PLoS One 8:e66166. https://doi.org/10.1371/journal.pone.0066166
29. Loncaric I, Kubber-Heiss A, Posautz A, Stalder GL, Hoffmann D, Rosengarten R, Walzer C. 2013. Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. J Antimicrob Chemother 68:2222-2225. https://doi.org/10.1093/jac/dkt186
30. Porrero MC, Mentaberre G, Sanchez S, Fernandez-Llario P, Casas-Diaz E, Mateos A, Vidal D, Lavin S, Fernandez-Garayzabal JF, Dominguez L. 2014. Carriage of Staphylococcus aureus by free-living wild animals in Spain. Appl Environ Microbiol 80:4865-4870. https://doi.org/10.1128/AEM.00647-14
31. Porrero MC, Valverde A, Fernandez-Llario P, Diez-Guerrier A, Mateos A, Lavin S, Canton R, Fernandez-Garayzabal JF, Dominguez L. 2014. Staphylococcus aureus carrying mecC gene in animals and urban wastewater, Spain. Emerg Infect Dis 20:899-901. https://doi.org/10.3201/eid2005.130426
32. Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K. 2006. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 188:2761-2773. https://doi.org/10.1128/JB.188.8.2761-2773.2006
33. Shahmirzadi SV, Nguyen MT, Götz F. 2016. Evaluation of Staphylococcus aureus lipoproteins: role in nutritional acquisition and pathogenicity. Front Microbiol 7:1404. https://doi.org/10.3389/fmicb.2016.01404
34. Penadés JR, Christie GE. 2015. The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu Rev Virol 2:181-201. https://doi.org/10.1146/annurev-virology-031413-085446
35. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K. 2002 Genome and virulence determinants of high virulence communityacquired MRSA. Lancet 359:1819-1827. https://doi.org/10.1016/S0140-6736(02)08713-5
36. Novick RP, Christie GE, Penadés JR. 2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541-551. https://doi.org/10.1038/nrmicro2393
37. Fu Z, Liu Y, Chen C, Guo Y, Ma Y, Yang Y, Hu F, Xu X, Wang M. 2016. Characterization of fosfomycin resistance gene, fosB, in methicillinresistant Staphylococcus aureus isolates. PLoS One 11:e0154829. https://doi.org/10.1371/journal.pone.0154829
38. Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ, Meaney WJ, Smyth CJ. 2001. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183:63-70. https://doi.org/10.1128/JB.183.1.63-70.2001
39. Chanda PK, Mondal R, Sau K, Sau S. 2009. Antibiotics, arsenate and H2O2 induce the promoter of Staphylococcus aureus cspC gene more strongly than cold. J Basic Microbiol 49:205-211. https://doi.org/10.1002/jobm.200800065
40. Kahánková J, Pantuček R, Goerke C, Ružičková V, Holochová P, Doškař J. 2010 Multilocus PCR typing strategy for differentiation of Staphylococcus aureus siphoviruses reflecting their modular genome structure. Environ Microbiol 12:2527-2538. https://doi.org/10.1111/j.1462-2920.2010.02226.x
41. Deghorain M, Bobay LM, Smeesters PR, Bousbata S, Vermeersch M, Perez-Morga D, Dreze PA, Rocha EP, Touchon M, Van Melderen L. 2012. Characterization of novel phages isolated in coagulase-negative staphylococci reveals evolutionary relationships with Staphylococcus aureus phages. J Bacteriol 194:5829-5839. https://doi.org/10.1128/JB.01085-12
42. Kim C, Milheirico C, Gardete S, Holmes MA, Holden MT, de Lencastre H, Tomasz A. 2012. Properties of a novel PBP2A protein homolog from Staphylococcus aureus strain LGA251 and its contribution to the betalactam-resistant phenotype. J Biol Chem 287:36854-36863. https://doi.org/10.1074/jbc.M112.395962
43. McRae CF, Hocking AD, Seppelt RD. 1999. Penicillium species from terrestrial habitats in the Windmill Islands, East Antarctica, including a new species, Penicillium antarcticum. Polar Biol 21:97-111. https://doi.org/10.1007/s003000050340
44. Montemartini Corte AM, Liotta M, Venturi CB, Calegari L. 2000. Antibacterial activity of Penicillium spp. strains isolated in extreme environments. Polar Biol 23:294-297. https://doi.org/10.1007/s003000050447
45. Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M, Frisvad JC, Onofri S. 2012. Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749-757. https://doi.org/10.1007/s00300-011-1119-6
46. Sonjak S, Frisvad JC, Gunde-Cimerman N. 2006. Penicillium mycobiota in arctic subglacial ice. Microb Ecol 52:207-216. https://doi.org/10.1007/s00248-006-9086-0
47. Godinho VM, Goncalves VN, Santiago IF, Figueredo HM, Vitoreli GA, Schaefer CE, Barbosa EC, Oliveira JG, Alves TM, Zani CL, Junior PA, Murta SM, Romanha AJ, Kroon EG, Cantrell CL, Wedge DE, Duke SO, Ali A, Rosa CA, Rosa LH. 2015. Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585-596. https://doi.org/10.1007/s00792-015-0741-6
48. Brunati M, Rojas JL, Sponga F, Ciciliato I, Losi D, Gottlich E, de Hoog S, Genilloud O, Marinelli F. 2009. Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genomics 2:43-50. https://doi.org/10.1016/j.margen.2009.04.002
49. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81-91. https://doi.org/10.1099/ijs.0.64483-0
50. Pantuček R, Švec P, Dajcs JJ, Machová I, Černohlávková J, Šedo O, Gelbíčová T, Mašlaňová I, Doškař J, Zdráhal Z, Ružičková V, Sedláček I. 2013 Staphylococcus petrasii sp. nov. including S. petrasii subsp. petrasii subsp. nov. and S. petrasii subsp. croceilyticus subsp. nov., isolated from human clinical specimens and human ear infections. Syst Appl Microbiol 36:90-95. https://doi.org/10.1016/j.syapm.2012.11.004
51. Mannerová S, Pantuček R, Doškař J, Švec P, Snauwaert C, Vancanneyt M, Swings J, Sedláček I. 2003. Macrococcus brunensis sp. nov., Macrococcus hajekii sp. nov. and Macrococcus lamae sp. nov., from the skin of llamas. Int J Syst Evol Microbiol 53:1647-1654. https://doi.org/10.1099/ijs.0.02683-0
52. The European Committee on Antimicrobial Susceptibility Testing. 2017. Breakpoint tables for interpretation of MICs and zone diameters, version 7.1. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_7.1_Breakpoint_Tables.pdf
53. CLSI. 2015. Performance standards for antimicrobial disk susceptibility tests; approved standard, 12th ed. CLSI document M02-A12. Clinical and Laboratory Standards Institute, Wayne, PA. https://clsi.org/standards/products/microbiology/documents/m02/
54. Sasser M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101. Microbial ID, Inc., Newark, DE
55. Švec P, Pantuček R, Petráš P, Sedláček I, Nováková D. 2010. Identification of Staphylococcus spp. using (GTG)5-PCR fingerprinting. Syst Appl Microbiol 33:451-456. https://doi.org/10.1016/j.syapm.2010.09.004
56. Pantuček R, Götz F, Doškař J, Rosypal S. 1996. Genomic variability of Staphylococcus aureus and the other coagulase-positive Staphylococcus species estimated by macrorestriction analysis using pulsed-field gel electrophoresis. Int J Syst Bacteriol 46:216-222. https://doi.org/10.1099/00207713-46-1-216
57. Pantuček R, Sedláček I, Petráš P, Koukalová D, Švec P, Ště tina V, Vancanneyt M, Chrastinová L, Vokurková J, Ružicková V, Doškař J, Swings J, Hájek V. 2005. Staphylococcus simiae sp. nov., isolated from South American squirrel monkeys. Int J Syst Evol Microbiol 55:1953-1958. https://doi.org/10.1099/ijs.0.63590-0
58. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y, Stepanauskas R, Clingenpeel SR, Woyke T, Mclean JS, Lasken R, Tesler G, Alekseyev MA, Pevzner PA. 2013. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20:714-737. https://doi.org/10.1089/cmb.2013.0084
59. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT. 2009. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25:2071-2073. https://doi.org/10.1093/bioinformatics/btp356
60. Wick RR, Schultz MB, Zobel J, Holt KE. 2015. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350-3352. https://doi.org/10.1093/bioinformatics/btv383
61. Okonechnikov K, Golosova O, Fursov M, UGENE Team. 2012. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166-1167. https://doi.org/10.1093/bioinformatics/bts091
62. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
63. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
64. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32-D36. https://doi.org/10.1093/nar/gkj014
65. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S. 2014. InterProScan 5: genome-scale protein function classification. Bioinformatics 30: 1236-1240. https://doi.org/10.1093/bioinformatics/btu031
66. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH. 2015 CDD: NCBI's conserved domain database. Nucleic Acids Res 43: D222-D226. https://doi.org/10.1093/nar/gku1221
67. Wang Y, Coleman-Derr D, Chen G, Gu YQ. 2015. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 43:W78-W84. https://doi.org/10.1093/nar/gkv487
68. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007 RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100-3108. https://doi.org/10.1093/nar/gkm160
69. Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874. https://doi.org/10.1093/molbev/msw054
70. Lee I, Kim YO, Park SC, Chun J. 2015. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol https://doi.org/10.1099/ijsem.0.000760
71. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M. 2013. Genome sequencebased species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
72. Calcutt MJ, Foecking MF, Hsieh HY, Perry J, Stewart GC, Middleton JR. 2013 Genome sequence analysis of Staphylococcus equorum bovine mastitis isolate UMC-CNS-924. Genome Announc 1:e00840-13. https://doi.org/10.1128/genomeA.00840-13
73. Zhou H, Yao Z, Shi H, Wang B, Li D, Hou J, Ma S. 2017. Draft genome sequence of Staphylococcus succinus subsp. succinus type strain DSM 14617, isolated from plant and soil inclusions within 25-to 35-million-year-old Dominican amber. Genome Announc 5:e01521-16. https://doi.org/10.1128/genomeA.01521-16
74. Shi D, Fang D, Hu X, Li A, Lv L, Guo J, Chen Y, Wu W, Guo F, Li L. 2015. Draft genome sequence of Staphylococcus gallinarum DSM 20610T, originally isolated from the skin of a chicken. Genome Announc 3:e00580-15. https://doi.org/10.1128/genomeA.00580-15
75. Shiroma A, Terabayashi Y, Nakano K, Shimoji M, Tamotsu H, Ashimine N, Ohki S, Shinzato M, Teruya K, Satou K, Hirano T. 2015. First complete genome sequences of Staphylococcus aureus subsp. aureus Rosenbach 1884 (DSM 20231T), determined by PacBio single-molecule real-time technology. Genome Announc 3:e00800-15. https://doi.org/10.1128/genomeA.00800-15