Skip to main content
Log in

A proposal to unify two subspecies of Staphylococcus equorum: Staphylococcus equorum subsp. equorum and Staphylococcus equorum subsp. linens

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Twelve isolates from jeotgal, a Korean high-salt-fermented seafood, identified as Staphylococcus equorum were compared by phenotypic and genotypic methods to determine their precise taxonomic identities at the subspecies level. Four strains and three strains had complete 16S rRNA gene sequence matches with S. equorum subsp. equorum DSM 20674T and S. equorum subsp. linens DSM 15097T, respectively. Five strains showed 99.9 % identity with the sequences of both type strains. In our DNA–DNA hybridization analyses among two type strains and two isolates, the similarities were over 72 % and were higher than the similarities presented at the subspecies proposal. Physiological characteristics such as sugar utilization, β-galactosidase activity, novobiocin resistance and salt tolerance, which were adopted for subspecies separation, could not be applied to assign the isolates to a taxonomic unit. Antibiotic susceptibility, hemolytic activity, biofilm formation and protein profiles did not present markers to divide the isolates into either of the subspecies. Multilocus sequence typing of the sequences of the 16S rRNA gene and five housekeeping genes did not produce any coherent relationship among the isolates and type strains. Repetitive element-PCR fingerprinting using ERIC (enterobacterial repetitive intergenic consensus) primers classified 12 isolates to three genotypes, and the genotypes of both type strains coincided with two isolates expressing different characteristics. Based on these phenotypic and genotypic analyses results, we propose to unify the present two subspecies of S. equorum into one species, S. equorum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adhikari RP, Arvidson S, Novick RP (2007) A nonsense mutation in agrA accounts for the defect in agr expression and the a virulence of Staphylococcus aureus 8325-4 traP:kan. Infect Immun 75:4534–4540

    Article  PubMed  CAS  Google Scholar 

  • Archer GL (1998) Staphylococcus aureus: a well-armed pathogen. Clin Infect Dis 26:1179–1181

    Article  PubMed  CAS  Google Scholar 

  • Brigante G, Menozzi MG, Pini B, Porta R, Somenzi P, Sciacca A, Spanu T, Stefani S (2008) Identification of coagulase-negative Staphylococci by using the BD phoenix system in the low-inoculum mode. J Clin Microbiol 46:3826–3828

    Article  PubMed  Google Scholar 

  • Chapman GH (1945) The significance of sodium chloride in studies of staphylococci. J Bacteriol 50:201–203

    CAS  Google Scholar 

  • Coton E, Mulder N, Coton M, Pochet S, Trip H, Lolkema JS (2010) Origin of the putrescine-producing ability of the coagulase-negative bacterium Staphylococcus epidermidis 2015B. Appl Environ Microbiol 76:5570–5576

    Article  PubMed  CAS  Google Scholar 

  • Duthie ES, Lorenz LL (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6:95–107

    Article  PubMed  CAS  Google Scholar 

  • Euzeby JP (2011) Definitaions and abbreviations. In: Euzeby JP (ed) List of Bacteria Names with Standing in Nomenclature. http://www.bacterio.cict.fr/s/staphylococcus.html

  • Götz F, Bannerman T, Schleifer K-H (2006) The Genera Staphylococcus and Macrococcus. Prokaryotes 4:5–75

    Article  Google Scholar 

  • Guan L, Cho KH, Lee JH (2011) Analysis of the cultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria. Food Microbiol 28:101–113

    Article  PubMed  CAS  Google Scholar 

  • Hammes WP, Hertel C (1998) New developments in meat starter cultures. Meat Sci 49S1:S125–S138

    Article  PubMed  CAS  Google Scholar 

  • Hebert GA, Hancock GA (1985) Synergistic hemolysis exhibited by species of staphylococci. J Clin Microbiol 22:409–415

    PubMed  CAS  Google Scholar 

  • Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091

    Article  PubMed  CAS  Google Scholar 

  • Irlinger F (2008) Safety assessment of dairy microorganisms: coagulase-negative staphylococci. Int J Food Microbiol 126:302–310

    Article  PubMed  CAS  Google Scholar 

  • Jeong DW, Cho H, Lee H, Li C, Garza J, Fried M, Bae T (2011) Identification of the P3 promoter and distinct roles of the two promoters of the SaeRS two-component system in Staphylococcus aureus. J Bacteriol 193:4672–4684

    Article  PubMed  CAS  Google Scholar 

  • Kacica MA, Horgan MJ, Preston KE, Lepow M, Venezia RA (1994) Relatedness of coagulase-negative staphylococci causing bacteremia in low-birthweight infants. Infect Control Hosp Epidemiol 15:658–662

    Article  PubMed  CAS  Google Scholar 

  • Kafatos FC, Jones CW, Efstratiadis A (1979) Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res 7:1541–1552

    Article  PubMed  CAS  Google Scholar 

  • Lane DJ (1991) 16S–23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  • Maiden MC (2006) Multilocus sequence typing of bacteria. Annu Rev Microbiol 60:561–588

    Article  PubMed  CAS  Google Scholar 

  • Miralles MC, Flores J, Perez-Martinez G (1996) Biochemical tests for the selection of Staphylococcus strains as potential meat starter cultures. Food Microbiol 13:227–236

    Article  CAS  Google Scholar 

  • Montel MC, Masson F, Talon R (1998) Bacterial role in flavour development. Meat Sci 49S1:S111–S123

    Article  PubMed  CAS  Google Scholar 

  • Natoli S, Fontana C, Favaro M, Bergamini A, Testore GP, Minelli S, Bossa MC, Casapulla M, Broglio G, Beltrame A, Cudillo L, Cerretti R, Leonardis F (2009) Characterization of coagulase-negative staphylococcal isolates from blood with reduced susceptibility to glycopeptides and therapeutic options. BMC Infect Dis 9:83

    Article  PubMed  Google Scholar 

  • Phillips WE Jr, Kloos WE (1981) Identification of coagulase-positive Staphylococcus intermedius and Staphylococcus hyicus subsp. hyicus isolates from veterinary clinical specimens. J Clin Microbiol 14:671–673

    PubMed  Google Scholar 

  • Place RB, Hiestand D, Gallmann HR, Teuber M (2003) Staphylococcus equorum subsp. linens, subsp. nov., a starter culture component for surface ripened semi-hard cheeses. Syst Appl Microbiol 26:30–37

    Article  PubMed  CAS  Google Scholar 

  • Schlegelova J, Babak V, Klimova E, Lukasova J, Navratilova P, Sustackova A, Sediva I, Rysanek D (2002) Prevalence of and resistance to anti-microbial drugs in selected microbial species isolated from bulk milk samples. J Vet Med B Infect Dis Vet Public Health 49:216–225

    Article  PubMed  CAS  Google Scholar 

  • Schleifer KH, Bell JA (2009) Staphylococcaceae family. nov. vol three. In: De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (eds) Bergey’s manual of systematic bacteriology. Springer, New York, p 392

    Google Scholar 

  • Schleifer KH, Kippler-Balz R, Devriese LA (1984) Staphylococcus arlettae sp. nov., S. equorum sp. nov. and S. kloosii sp. nov.: three new coagulase-negative, novobiocin-resistant species from animals. Syst Appl Microbiol 5:501–509

    Article  Google Scholar 

  • Traber K, Novick R (2006) A slipped-mispairing mutation in AgrA of laboratory strains and clinical isolates results in delayed activation of agr and failure to translate delta- and alpha-haemolysins. Mol Microbiol 59:1519–1530

    Article  PubMed  CAS  Google Scholar 

  • Vandenesch F, Lebeau C, Bes M, Lina G, Lina B, Greenland T, Benito Y, Brun Y, Fleurette J, Etienne J (1994) Clotting activity in Staphylococcus schleiferi subspecies from human patients. J Clin Microbiol 32:388–392

    PubMed  CAS  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Truper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Widerstrom M, Wistrom J, Sjostedt A, Monsen T (2012) Coagulase-negative 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

    Article  PubMed  CAS  Google Scholar 

  • Wieser M, Busse HJ (2000) Rapid identification of Staphylococcus epidermidis. Int J Syst Evol Microbiol 50:1087–1093

    Article  PubMed  CAS  Google Scholar 

  • Witte W (2000) Ecological impact of antibiotic use in animals on different complex microflora: environment. Int J Antimicrob Agents 14:321–325

    Article  PubMed  CAS  Google Scholar 

  • Woo PC, Leung AS, Leung KW, Yuen KY (2001) Identification of slide coagulase positive, tube coagulase negative Staphylococcus aureus by 16S ribosomal RNA gene sequencing. Mol Pathol 54:244–247

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by R&D Convergence Center Support Program, Ministry of Agriculture, Food and Rural Affairs, Republic of Korea and supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2012R1A1A2039955). This work (Seulhwa Han) was supported by Kyonggi University Research Assistant Fellowship 2012.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jong-Hoon Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jeong, DW., Kim, HR., Han, S. et al. A proposal to unify two subspecies of Staphylococcus equorum: Staphylococcus equorum subsp. equorum and Staphylococcus equorum subsp. linens . Antonie van Leeuwenhoek 104, 1049–1062 (2013). https://doi.org/10.1007/s10482-013-0025-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-013-0025-z

Keywords

Navigation