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Monteiro Marques, J.; Coelho, M.; Santana, A.R.; Pinto, D.; Semedo-Lemsaddek, T. Enterococcal Genetic Lineages. Encyclopedia. Available online: https://encyclopedia.pub/entry/47844 (accessed on 10 September 2024).
Monteiro Marques J, Coelho M, Santana AR, Pinto D, Semedo-Lemsaddek T. Enterococcal Genetic Lineages. Encyclopedia. Available at: https://encyclopedia.pub/entry/47844. Accessed September 10, 2024.
Monteiro Marques, Joana, Mariana Coelho, Andressa Rodrigues Santana, Daniel Pinto, Teresa Semedo-Lemsaddek. "Enterococcal Genetic Lineages" Encyclopedia, https://encyclopedia.pub/entry/47844 (accessed September 10, 2024).
Monteiro Marques, J., Coelho, M., Santana, A.R., Pinto, D., & Semedo-Lemsaddek, T. (2023, August 09). Enterococcal Genetic Lineages. In Encyclopedia. https://encyclopedia.pub/entry/47844
Monteiro Marques, Joana, et al. "Enterococcal Genetic Lineages." Encyclopedia. Web. 09 August, 2023.
Enterococcal Genetic Lineages
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This entry is adapted from the peer-reviewed paper 10.3390/antibiotics12071140

Enterococcus spp. are commensals of the gastrointestinal tracts of humans and animals and colonize a variety of niches such as water, soil, and food. Over the last three decades, enterococci have evolved as opportunistic pathogens, being considered ESKAPE pathogens responsible for hospital-associated infections. E. faecalis and E. faecium exhibit conserved genomes, although they possess a significant accessory genome (up to 38% in E. faecium), which contributes to remarkable genomic plasticity. The evolution of enterococci was predominantly influenced by recombination and proficiency in acquiring novel genes through HGT facilitated by MGEs, such as plasmids, transposons, genomic islands (GI), and prophages.

Enterococcus genetic lineages virulence factors antimicrobial resistance

1. Enterococcus spp.—An Overview

Enterococcus spp. are ubiquitous gram-positive cocci that inhabit the normal intestinal microbiota of humans and animals and colonize a variety of environmental sources such as soils, water, and fresh and fermented foods. These facultative anaerobes, catalase-negative, non-spore-forming bacteria can tolerate high salt concentrations (6.5% NaCl), wide pH values (4.5–10.0), and growth temperatures ranging from 10 to 45 °C (optimal at 36 °C) and present variable resistance to chemical disinfectants, such as alcohol and chlorhexidine [1][2][3]. In fact, enterococci possess remarkable stress resilience, which can be enhanced by exposure to sublethal harsh conditions, surviving temperatures as high as 60 °C, desiccation in the environment, and starvation [4]. In addition, enterococci are known to hydrolyze esculin in the presence of 40% bile salts [1][2]. As homofermentative bacteria, they produce lactic acid from glucose fermentation without gas production [2]. Likewise, enterococci play a significant role in the organoleptic properties of fermented foods, due to their natural occurrence as contaminants in raw and dairy food products, resistance to food processing conditions (thermotolerance), low toxicity, and ability to acidify the environment [2]. These attributes are crucial for successful use in food fermentation processes, either as starter or non-starter bacteria, and inclusion in probiotic formulations [5].
However, enterococci have emerged as relevant opportunistic pathogens in the last decades, representing a major cause of healthcare-associated infections due to rapid adaptation to the host and ability to acquire a diversity of virulence and antibiotic resistance genes (ARGs; resistome [6]) through horizontal gene transfer (HGT), largely mediated by mobile genetic elements (MGEs; composing the mobilome) [7]. These bacteria can cause a variety of infections in humans (urinary tract, intra-abdominal, and tissue infections; bacteremia, and endocarditis [8]) and animals (urinary tract infection, otitis externa, peritonitis, endocarditis, and mastitis in dairy animals [9]). Among the growing number of enterococcal species identified, Enterococcus faecalis and E. faecium are the most common infection-related species, with E. faecalis accounting for the majority of infections [10]. Yet, the proportion of E. faecium infections has been progressively increasing, due to the spread of antimicrobial resistance (AMR), particularly vancomycin-resistant E. faecium (VREfm), which has been responsible for the majority of vancomycin-resistant enterococci (VRE) outbreaks worldwide [11][12]. According to recent evidence, the percentage of clinical VREfm varies between 1 and 46.3% in Europe, 75 and 80% in the USA, and 11.3 and 75% in Australia [11]. These increased levels of resistance have led to the inclusion of VREfm in the high-priority pathogens list, defined by the World Health Organization (WHO) and the ESKAPE pathogen group formed by E. faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp. [13][14]. Other relevant species of the enterococcal genus include E. avium, E. gallinarum, E. casseliflavus, E. hirae, E. mundtii, and E. raffinosus, E. gallinarum and E. casseliflavus being of special interest, due to their intrinsic resistance to vancomycin [2]. In general, it has been estimated that enterococci represent 6.1–17.5% of the total number of isolates obtained from European patients carrying hospital-acquired infections between 2010 and 2020 [15].

2. Genetic Lineages

E. faecalis and E. faecium exhibit conserved genomes, although they possess a significant accessory genome (up to 38% in E. faecium), which contributes to remarkable genomic plasticity [16]. The evolution of enterococci was predominantly influenced by recombination and proficiency in acquiring novel genes through HGT facilitated by MGEs, such as plasmids, transposons [16][17], genomic islands (GI), and prophages [18]. The genome plasticity of clinical E. faecium can be explained by the lack of genome defense mechanisms limiting HGT, such as CRISPR–Cas and restriction-modification systems [16]. Accordingly, an inverse correlation between the presence of the CRISPR–Cas locus and acquired antimicrobial resistance in E. faecalis was first demonstrated in 2010 [19]. Recently, the lack of CRISPR–Cas genes was also associated with higher antimicrobial resistance rates and multidrug resistance in E. faecalis and E. faecium originating from hospital wastewater [20].
The duality between commensals and infection-causing organisms, and the remarkable adaptability to various environmental sources, led to the division of E. faecium into two distinct genomic clades: clade A, encompassing hospital-associated lineages (e.g., vancomycin-resistant isolates); and clade B, comprising community-associated enterococci [3][21][22]. However, the discovery of clinical isolates within the clade B lineage led some authors to challenge this classification [23]. Palmer et al. [17] pointed out two evolutionary theories to explain the emergence of the two clades. The first is that clade A and clade B may be endogenous to the gastrointestinal tracts of different hosts and now coexist among human microbiota, as a result of antibiotic elimination of competitors. The other is that clades A and B may be diverging from each other, due to antibiotic use and ecological isolation, although this is less likely [17]. Clade A can be further classified into two distinct sub-clades: clade A1, consisting of human clinical epidemic strains, which account for the majority of human infections (mostly referred to as CC17, further explored in Section 4); and clade A2, typically associated with livestock/animal strains and some occasional human infection isolates [22]. Interestingly, some animal-origin enterococci found in clade A1 were isolated from pet dogs, suggesting an interconnection between hospital strains and household pets [22]. In fact, an additional study demonstrated that sub-clade A1 emerged from A2, and that hospital isolates identified as A2 represent a genetic continuum between A1 and community E. faecium placed in clade B [7]. Thus, the existence of this sub-clade division has been contested and remains uncertain [7][23].
In comparison to E. faecium, E. faecalis isolates do not exhibit a multiclade structure, instead displaying a significant reliance on the acquisition of mobile elements as a primary driver of genomic diversity [17]. Nevertheless, some major high-risk enterococcal clonal complexes (HiRECCs), namely CC2, CC9, and CC87 (further explored in Section 4), have been associated to hospital settings and healthcare-associated infections [1][24]. Enterococci express various fitness and adaptive factors, referring to cumulative evolutionary mechanisms that allow them to survive and thrive in high-pressure selective environments (e.g., healthcare facilities and food industries). 

References

  1. Geraldes, C.; Tavares, L.; Gil, S.; Oliveira, M. Enterococcus Virulence and Resistant Traits Associated with Its Permanence in the Hospital Environment. Antibiotics 2022, 11, 857.
  2. Lebreton, F.; Willems, R.J.L.; Gilmore, M.S. Enterococcus Diversity, Origins in Nature, and Gut Colonization. In Enterococci: From Commensals to Leading Causes of Drug Resistant Infection; Massachusetts Eye and Ear Infirmary: Boston, MA, USA, 2014; pp. 1–46.
  3. Lee, T.; Pang, S.; Abraham, S.; Coombs, G.W. Antimicrobial-Resistant CC17 Enterococcus faecium: The Past, the Present and the Future. J. Glob. Antimicrob. Resist. 2019, 16, 36–47.
  4. Lebreton, F.; Manson, A.L.; Saavedra, J.T.; Straub, T.J.; Earl, A.M.; Gilmore, M.S. Tracing the Enterococci from Paleozoic Origins to the Hospital. Cell 2017, 169, 849–861.
  5. Krawczyk, B.; Wityk, P.; Gałęcka, M.; Michalik, M. The Many Faces of Enterococcus spp.—Commensal, Probiotic and Opportunistic Pathogen. Microorganisms 2021, 9, 1900.
  6. Kim, D.W.; Cha, C.J. Antibiotic Resistome from the One-Health Perspective: Understanding and Controlling Antimicrobial Resistance Transmission. Exp. Mol. Med. 2021, 53, 301–309.
  7. van Hal, S.J.; Willems, R.J.L.; Gouliouris, T.; Ballard, S.A.; Coque, T.M.; Hammerum, A.M.; Hegstad, K.; Pinholt, M.; Howden, B.P.; Malhotra-Kumar, S.; et al. The Interplay between Community and Hospital Enterococcus faecium Clones within Health-Care Settings: A Genomic Analysis. Lancet Microbe 2022, 3, e133–e141.
  8. Semedo, T.; Almeida Santos, M.; Silva Lopes, M.F.; Figueiredo Marques, J.J.; Barreto Crespo, M.T.; Tenreiro, R. Virulence Factors in Food, Clinical and Reference Enterococci: A Common Trait in the Genus? Syst. Appl. Microbiol. 2003, 26, 13–22.
  9. Stępień-Pyśniak, D.; Bertelloni, F.; Dec, M.; Cagnoli, G.; Pietras-Ożga, D.; Urban-Chmiel, R.; Ebani, V.V. Characterization and Comparison of Enterococcus spp. Isolates from Feces of Healthy Dogs and Urine of Dogs with UTIs. Animals 2021, 11, 2845.
  10. Hashem, Y.A.; Abdelrahman, K.A.; Aziz, R.K. Phenotype–Genotype Correlations and Distribution of Key Virulence Factors in Enterococcus faecalis Isolated from Patients with Urinary Tract Infections. Infect. Drug Resist. 2021, 14, 1713–1723.
  11. Zhou, X.; Willems, R.J.L.; Friedrich, A.W.; Rossen, J.W.A.; Bathoorn, E. Enterococcus faecium: From Microbiological Insights to Practical Recommendations for Infection Control and Diagnostics. Antimicrob. Resist. Infect. Control. 2020, 9, 1–13.
  12. Markwart, R.; Willrich, N.; Haller, S.; Noll, I.; Koppe, U.; Werner, G.; Eckmanns, T.; Reuss, A. The Rise in Vancomycin-Resistant Enterococcus faecium in Germany: Data from the German Antimicrobial Resistance Surveillance (ARS). Antimicrob. Resist. Infect. Control. 2019, 8, 1–11.
  13. Denissen, J.; Reyneke, B.; Waso-Reyneke, M.; Havenga, B.; Barnard, T.; Khan, S.; Khan, W. Prevalence of ESKAPE Pathogens in the Environment: Antibiotic Resistance Status, Community-Acquired Infection and Risk to Human Health. Int. J. Hyg. Environ. Health 2022, 244, 1–17.
  14. Rice, L.B. Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE. J. Infect. Dis. 2008, 197, 1079–1081.
  15. Brinkwirth, S.; Ayobami, O.; Eckmanns, T.; Markwart, R. Hospital-Acquired Infections Caused by Enterococci: A Systematic Review and Meta-Analysis, Who European Region, 1 January 2010 to 4 February 2020. Eurosurveillance 2021, 26, 1–16.
  16. Cattoir, V. The Multifaceted Lifestyle of Enterococci: Genetic Diversity, Ecology and Risks for Public Health. Curr. Opin. Microbiol. 2022, 65, 73–80.
  17. Palmer, K.L.; Godfrey, P.; Griggs, A.; Kos, V.N.; Zucker, J.; Desjardins, C.; Cerqueira, G.; Gevers, D.; Walker, S.; Wortman, J.; et al. Comparative Genomics of Enterococci: Variation in Enterococcus faecalis, Clade Structure in E. Faecium, and Defining Characteristics of E. gallinarum and E. casseliflavus. mBio 2012, 3, 1–11.
  18. Sanderson, H.; Gray, K.L.; Manuele, A.; Maguire, F.; Khan, A.; Liu, C.; Navanekere Rudrappa, C.; Nash, J.H.E.; Robertson, J.; Bessonov, K.; et al. Exploring the Mobilome and Resistome of Enterococcus faecium in a One Health Context across Two Continents. Microb. Genom. 2022, 8, 1–17.
  19. Palmer, K.L.; Gilmore, M.S. Multidrug-Resistant Enterococci Lack CRISPR-Cas. mBio 2010, 1, 1–10.
  20. Alduhaidhawi, A.H.M.; Alhuchaimi, S.N.; Al-Mayah, T.A.; Al-Ouqaili, M.T.S.; Alkafaas, S.S.; Muthupandian, S.; Saki, M. Prevalence of CRISPR-Cas Systems and Their Possible Association with Antibiotic Resistance in Enterococcus faecalis and Enterococcus faecium Collected from Hospital Wastewater. Infect. Drug Resist. 2022, 15, 1143–1154.
  21. Galloway-Peña, J.; Roh, J.H.; Latorre, M.; Qin, X.; Murray, B.E. Genomic and SNP Analyses Demonstrate a Distant Separation of the Hospital and Community-Associated Clades of Enterococcus faecium. PLoS ONE 2012, 7, 1–10.
  22. Lebreton, F.; van Schaik, W.; McGuire, A.M.; Godfrey, P.; Griggs, A.; Mazumdar, V.; Corander, J.; Cheng, L.; Saif, S.; Young, S.; et al. Emergence of Epidemic Multidrug-Resistant Enterococcus faecium from Animal and Commensal Strains. mBio 2013, 4, 1–10.
  23. Raven, K.E.; Reuter, S.; Reynolds, R.; Brodrick, H.J.; Russell, J.E.; Török, M.E.; Parkhill, J.; Peacock, S.J. A Decade of Genomic History for Healthcare-Associated Enterococcus faecium in the United Kingdom and Ireland. Genome Res. 2016, 26, 1388–1396.
  24. Leavis, H.L.; Bonten, M.J.; Willems, R.J. Identification of High-Risk Enterococcal Clonal Complexes: Global Dispersion and Antibiotic Resistance. Curr. Opin. Microbiol. 2006, 9, 454–460.
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Subjects: Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Joana Monteiro Marques
,
Mariana Coelho
,
Andressa Rodrigues Santana
,
Daniel Pinto
,
Teresa Semedo-Lemsaddek
View Times: 273
Revisions: 2 times (View History)
Update Date: 11 Aug 2023
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