Serratia marcescens: микробиологическая характеристика, резистентные свойства, вирулентность и клиническая значимость

Serratia marcescens (SM) относится к актуальным возбудителям оппортунистических инфекций. Обзор содержит анализ данных, посвящённых значению SM в медицинской практике. Подробно проанализированы молекулярно-генетические предикторы вирулентности и антибиотикорезистентности этого патогена. Рассматриваются основные методы типирования SM. Описаны разнообразные формы инфекций, вызываемых SM, — как локальные, так и генерализованные.

Участие авторов:
Садеева З.З., Лазарева А.В. — концепция и дизайн исследования, написание текста;
Садеева З.З., Новикова И.Е., Алябьева Н.М. — сбор и обработка материала;
Лазарева А.В., Алябьева Н.М. — редактирование.
Все соавторы — утверждение окончательного варианта статьи, ответственность за целостность всех частей статьи.

Финансирование. Исследование не имело финансовой поддержки.

Конфликт интересов. Авторы заявляют об отсутствии конфликта интересов. 

Поступила 26.04.2023
Принята к печати 16.05.2023
Опубликована 27.06.2023

1. Abreo E., Altier N. Pangenome of Serratia marcescens strains from nosocomial and environmental origins reveals different populations and the links between them. Sci. Rep. 2019; 9(1): 46. https://doi.org/10.1038/s41598-018-37118-0

2. Breijyeh Z., Jubeh B., Karaman R. Resistance of gram-negative bacteria to current antibacterial agents and approaches to resolve it. Molecules. 2020; 25(6): 1340. https://doi.org/10.3390/molecules25061340

3. Grimont P.A., Grimont F. The genus Serratia. Annu. Rev. Microbiol. 1978; 32: 221–48. https://doi.org/10.1146/annurev.mi.32.100178.001253

4. Покровский В.И. Энтеробактерии. М.: Медицина; 1985.

5. Mahlen S.D. Serratia infections: from military experiments to current practice. Clin. Microbiol. Rev. 2011; 24(4): 755–91. https://doi.org/10.1128/CMR.00017-11

6. Petersen L.M., Tisa L.S. Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Can. J. Microbiol. 2013; 59(9): 627–40. https://doi.org/10.1139/cjm-2013-0343

7. Benagli C., Rossi V., Dolina M., Tonolla M., Petrini O. Matrix-assisted laser desorption ionization-time of flight mass spectrometry for the identification of clinically relevant bacteria. PLoS One. 2011; 6(1): e16424. https://doi.org/10.1371/journal.pone.0016424

8. Zhang C., Yu Z., Zhang M., Li X., Wang M., Li L., et al. Serratia marcescens PLR enhances lateral root formation through supplying PLR-derived auxin and enhancing auxin biosynthesis in Arabidopsis. J. Exp. Bot. 2022; 73(11): 3711–25. https://doi.org/10.1093/jxb/erac074

9. Starr M.P., Grimont P.A., Grimont F., Starr P.B. Caprylate-thallous agar medium for selectively isolating Serratia and its utility in the clinical laboratory. J. Clin. Microbiol. 1976; 4(3): 270–6. https://doi.org/10.1128/jcm.4.3.270-276.1976

10. Bourdin T., Monnier A., Benoit M.È., Bédard E., Prévost M., Quach C., et al. A high-throughput short sequence typing scheme for Serratia marcescens pure culture and environmental DNA. Appl. Environ. Microbiol. 2021; 87(24): e0139921. https://doi.org/10.1128/AEM.01399-21

11. Besler K.R., Little E.L. Diversity of Serratia marcescens strains associated with cucurbit yellow vine disease in Georgia. Plant Dis. 2017; 101(1): 129–36. https://doi.org/10.1094/PDIS-05-16-0618-RE

12. Kampmeier S., Prior K., Cunningham S.A., Goyal A., Harmsen D., Patel R., et al. Development and evaluation of a core genome Multilocus Sequencing Typing (cgMLST) scheme for Serratia marcescens molecular surveillance and outbreak investigations. J. Clin. Microbiol. 2022; 60(11): e0119622. https://doi.org/10.1128/jcm.01196-22

13. Xu Q., Fu Y., Zhao F., Jiang Y., Yu Y. Molecular characterization of carbapenem-resistant serratia marcescens clinical isolates in a tertiary hospital in Hangzhou, China. Infect. Drug Resist. 2020; 13: 999–1008. https://doi.org/10.2147/IDR.S243197

14. Ruiz-Sada P., Escalante M., Lizarralde E. Severe acute infection due to Serratia marcescens causing respiratory distress in an immunocompetent adult. Rom. J. Intern. Med. 2016; 54(2): 134–6. https://doi.org/10.1515/rjim-2016-0013

15. AMRbook. База данных о резистентности. Available at: https://amrbook.ru/activity

16. Bolourchi N., Goodarzi N., Giske C.G., Nematzadeh S., Haririzadeh Jouriani F., Solgi H., et al. Comprehensive pan-genomic, resistome and virulome analysis of clinical OXA-48 producing carbapenem-resistant Serratia marcescens strains. Gene. 2022; 822: 146355. https://doi.org/10.1016/j.gene.2022.146355

17. Iguchi A., Nagaya Y., Pradel E., Ooka T., Ogura Y., Katsura K., et al. Genome evolution and plasticity of Serratia marcescens, an important multidrug-resistant nosocomial pathogen. Genome. Biol. Evol. 2014; 6(8): 2096–110. https://doi.org/10.1093/gbe/evu160

18. Zhao W.H., Hu Z.Q., Chen G., Matsushita K., Fukuchi K., Shimamura T. Characterization of imipenem-resistant Serratia mar­cescens producing IMPtype and TEM-type β-lactamases encoded on a single plasmid. Microbiol. Res. 2007; 162(1): 46–52. https://doi.org/10.1016/j.micres.2006.06.005

19. da Costa Guimarães A.C., Almeida A.C., Nicoletti A.G., Vilela M.A., Gales A.C., de Morais M.M. Clonal spread of carbapenem-resistant Serratia marcescens isolates sharing an IncK plasmid containing blaKPC-2. Int. J. Antimicrob. Agents. 2013; 42(4): 369–70. https://doi.org/10.1016/j.ijantimicag.2013.05.017

20. Sands K., Carvalho M.J., Portal E., Thomson K., Dyer C., Akpulu C., et al. Characterization of antimicrobial-resistant Gram-negative bacteria that cause neonatal sepsis in seven low- and middle-income countries. Nat. Microbiol. 2021; 6(4): 512–23. https://doi.org/10.1038/s41564-021-00870-7

21. Сидоренко С.В., Тишков В.И. Молекулярные основы резис­тентности к антибиотикам. Успехи биологической химии. 2004; 44(2): 263–306.

22. Gruber T.M., Göttig S., Mark L., Christ S., Kempf V.A., Wichelhaus T.A., et al. Pathogenicity of pan-drug-resistant Serratia marcescens harbouring blaNDM-1. J. Antimicrob. Chemother. 2015; 70(4): 1026–30. https://doi.org/10.1093/jac/dku482

23. Bidwell J.L., Reeves D.S., Bullock D.V. Diversity of R-plasmids in epidemic Serratia marcescens from the South West of Ingland. In: New Trends in Antibiotics: Research and Therapy. Amsterdam: Elsevier; 1981: 268–70.

24. Létoffé S., Ghigo J.M., Wandersman C. Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc. Natl. Acad. Sci. USA. 1994; 91(21): 9876–80. https://doi.org/10.1073/pnas.91.21.9876

25. Kanonenberg K., Schwarz C.K., Schmitt L. Type I secretion systems – a story of appendices. Res. Microbiol. 2013; 164(6): 596–604. https://doi.org/10.1016/j.resmic.2013.03.011

26. Korotkov K.V., Sandkvist M., Hol W.G. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 2012; 10(5): 336–51. https://doi.org/10.1038/nrmicro2762

27. Grijpstra J., Arenas J., Rutten L., Tommassen J. Autotransporter secretion: varying on a theme. Res. Microbiol. 2013; 164(6): 562–82. https://doi.org/10.1016/j.resmic.2013.03.010

28. Piccirilli A., Cherubini S., Brisdelli F., Fazii P., Stanziale A., Di Valerio S., et al. Molecular characterization by whole-genome sequencing of clinical and environmental Serratia marcescens strains isolated during an outbreak in a Neonatal Intensive Care Unit (NICU). Diagnostics (Basel). 2022; 12(9): 2180. https://doi.org/10.3390/diagnostics12092180

29. Лабинская А.С., Костюкова Н.Н., ред. Руководство по медицинской микробиологии. Книга III. Том первый. Оппортунистические инфекции: возбудители и этиологическая диагностика. М.: БИНОМ; 2020: 243–86.

30. Shimuta K., Ohnishi M., Iyoda S., Gotoh N., Koizumi N., Watanabe H. The hemolytic and cytolytic activities of Serratia marcescens phospholipase A (PhlA) depend on lysophospholipid production by PhlA. BMC Microbiol. 2009; 9: 261. https://doi.org/10.1186/1471-2180-9-261

31. Han R., Xiang R., Li J., Wang F., Wang C. High-level production of microbial prodigiosin: A review. J. Basic Microbiol. 2021; 61(6): 506–23. https://doi.org/10.1002/jobm.202100101

32. Haddix P.L., Jones S., Patel P., Burnham S., Knights K., Powell J.N., et al. Kinetic analysis of growth rate, ATP, and pigmentation suggests an energy-spilling function for the pigment prodigiosin of Serratia marcescens. J. Bacteriol. 2008; 190(22): 7453–63. https://doi.org/10.1128/JB.00909-08

33. Buttinelli E., Ardoino I., Lanzoni M., Domeniconi G., Pugni L., Ronchi A., et al. Epidemiology of Serratia marcescens infections in NICU of a teaching and research hospital in Northern Italy. Minerva Pediatr. (Torino). 2023; 75(2): 180–7. https://doi.org/10.23736/s2724-5276.17.04856-3

34. Shanks R.M., Stella N.A., Kalivoda E.J., Doe M.R., O’Dee D.M., Lathrop K.L., et al. A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J. Bacteriol. 2007; 189(20): 7262–72. https://doi.org/10.1128/JB.00859-07

35. Khaitlina S., Bozhokina E., Tsaplina O., Efremova T. Bacterial actin-specific endoproteases grimelysin and protealysin as virulence factors contributing to the invasive activities of Serratia. Int. J. Mol. Sci. 2020; 21(11): 4025. https://doi.org/10.3390/ijms21114025

36. Zhang L., Morrison A.J., Thibodeau P.H. Interdomain contacts and the stability of Serralysin protease from Serratia marcescens. PLoS One. 2015; 10(9): e0138419. https://doi.org/10.1371/journal.pone.0138419

37. Akatsuka H., Binet R., Kawai E., Wandersman C., Omori K. Lipase secretion by bacterial hybrid ATP-binding cassette exporters: molecular recognition of the LipBCD, PrtDEF, and HasDEF expor­ters. J. Bacteriol. 1997; 179(15): 4754–60. https://doi.org/10.1128/jb.179.15.4754-4760.1997

38. Pineda-Castellanos M.L., Rodríguez-Segura Z., Villalobos F.J., Hernández L., Lina L., Nuñez-Valdez M.E. Pathogenicity of isolates of Serratia marcescens towards larvae of the scarab Phyllophaga blanchardi (Coleoptera). Pathogens. 2015; 4(2): 210–28. https://doi.org/10.3390/pathogens4020210

39. Bruna R.E., Molino M.V., Lazzaro M., Mariscotti J.F., García Véscovi E. CpxR-dependent thermoregulation of Serratia marcescens PrtA metalloprotease expression and its contribution to bacterial biofilm formation. J. Bacteriol. 2018; 200(8): e00006–18. https://doi.org/10.1128/JB.00006-18

40. Choe H.S., Son S.W., Choi H.A., Kim H.J., Ahn S.G., Bang J.H., et al. Analysis of the distribution of bacteria within urinary catheter biofilms using four different molecular techniques. Am. J. Infect. Control. 2012; 40(9): e249–e254. https://doi.org/10.1016/j.ajic.2012.05.010

41. Robertson D., Patel N., Hinojosa J., Zhu M. Microbial colonization of contact lens surfaces in the presence of neutrophils. Contact Lens and Anterior Eye. 2018; 41(Suppl. 1): S20. https://doi.org/10.1016/j.clae.2018.04.144

42. Moles L., Gómez M., Moroder E., Jiménez E., Escuder D., Bustos G., et al. Serratia marcescens colonization in preterm neonates during their neonatal intensive care unit stay. Antimicrob. Resist. Infect. Control. 2019; 8: 135. https://doi.org/10.1186/s13756-019-0584-5

43. Fekrirad Z., Gattali B., Kashef N. Quorum sensing-regulated functions of Serratia marcescens are reduced by eugenol. Iran. J. Microbiol. 2020; 12(5): 451–9. https://doi.org/10.18502/ijm.v12i5.4607

44. Abbas H.A., Elsherbini A.M. Silencing the nosocomial pathogen Serratia marcescens by glyceryl trinitrate. Afr. Health Sci. 2018; 18(1): 1–10. https://doi.org/10.4314/ahs.v18i1.2

45. Brouqui P., Raoult D. Endocarditis due to rare and fastidious bacteria. Clin. Microbiol. Rev. 2001; 14(1): 177–207. https://doi.org/10.1128/CMR.14.1.177-207.2001

46. Elkattawy S., Mohammadian M., Williams N., Mowafy A., Ayad S., Noori M.A.M., et al. Serratia marcescens endocarditis. Cureus. 2021; 13(8): e17346. https://doi.org/10.7759/cureus.17346

47. Momose T., Masutani S., Oshima A., Kawasaki H., Tanaka R., Iwamoto Y., et al. First pediatric case of infective endocarditis caused by Serratia liquefaciens. Int. Heart J. 2018; 59(6): 1485–7. https://doi.org/10.1536/ihj.17-595

48. Cilli F., Nazli-Zeka A., Arda B., Sipahi O.R., Aksit-Barik S., Kepeli N., et al. Serratia marcescens sepsis outbreak caused by contaminated propofol. Am. J. Infect. Control. 2019; 47(5): 582–4. https://doi.org/10.1016/j.ajic.2018.10.014

49. González Sanchidrián S., Marín Álvarez J.P., Deira Lorenzo J., Labrador Gómez P.J., Gómez-Martino Arroyo J.R. Serratia marcescens bacteraemia outbreak in hemodialysis. Comment on «Serratia marcescens bacteraemia outbreak in haemodialysis patients with tunnelled catheters due to colonisation of antiseptic solution. Experience from 4 hospitals». Nefrologia (Engl. Ed.). 2018; 38(1): 94–6. https://doi.org/10.1016/j.nefro.2016.12.003

50. Ersoz G., Uguz M., Aslan G., Horasan E.S., Kaya A. Outbreak of meningitis due to Serratia marcescens after spinal anaesthesia. J. Hosp. Infect. 2014; 87(2): 122–5. https://doi.org/10.1016/j.jhin.2014.03.004

51. Papazoglou N., Samarkos M., Vergadis C., Cholongitas E. Abdominal aorta aneurysm endograft infection mimicking bacteraemic urinary tract infection. Hippokratia. 2021; 25(2): 91–3.