Skip to main content
Log in

Current trends of human infections and antibiotic resistance of the genus Shewanella

  • Review
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Shewanella spp. are commonly known as environmental bacteria and are most frequently isolated from aquatic areas. Currently, diseases syndromes and multidrug resistance have increasingly been reported in the genus Shewanella. Some species are associated with various infections, such as skin and soft tissue infections, as well as bacteremia. Generally, these bacteria are opportunistic and mostly affect people with an impaired immune system. This genus is also a probable vehicle and progenitor of antibiotic resistance genes. In fact, several resistance genes and mobile genetic elements have been identified in some resistant species isolated from environmental or clinical settings. These genes confer resistance to different antibiotic classes, including those used in therapies such as β-lactams and quinolones, and are generally located on the chromosome. Recently, a multidrug-resistant (MDR) plasmid harboring several drug resistance genes associated with transposons and integrons has been identified in Shewanella xiamenensis. These antibiotic resistance genes can circulate in the environment and contribute to the emergence of antibiotic resistance. This review describes different aspects of Shewanella, focusing on the infections caused by this genus, as well as their role in the propagation of antibiotic resistance via mobile genetic elements.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Satomi M (2014) The family Shewanellaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes, 4th edn. Springer, Heidelberg New York Dordrecht London

    Google Scholar 

  2. Janda JM (2014) Shewanella: a marine pathogen as an emerging cause of human disease. Clin Microbiol Newsl 36:25–29

    Article  Google Scholar 

  3. Poirel L, Héritier C, Nordmann P (2004) Chromosome-encoded ambler class D β-lactamase of Shewanella oneidensis as a progenitor of carbapenem-hydrolyzing oxacillinase. Antimicrob Agents Chemother 48:348–351. doi:10.1128/AAC.48.1.348-351.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Potron A, Poirel L, Nordmann P (2011) Origin of OXA-181, an emerging carbapenem-hydrolyzing oxacillinase, as a chromosomal gene in Shewanella xiamenensis. Antimicrob Agents Chemother 55:4405–4407. doi:10.1128/AAC.00681-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yousfi K, Touati A, Lefebvre B, Fournier É, Côté JC, Soualhine H, Walker M, Bougdour D, Tremblay C, Bekal S (2016) A novel plasmid, pSx1, harboring a new Tn1696 derivative from extensively drug-resistant Shewanella xiamenensis encoding OXA-416. Microb Drug Resist. doi:10.1089/mdr.2016.0025

    Google Scholar 

  6. Levin RE (1972) Correlation of DNA base composition and metabolism of Pseudomonas putrefaciens isolates from food, human clinical specimens, and other sources. Antonie Van Leeuwenhoek 38:121–127

    Article  CAS  PubMed  Google Scholar 

  7. Lee JV, Gibson DM, Shewan JM (1977) A numerical taxonomic study of some Pseudomonas-like marine bacteria. J Gen Microbiol 98:439–451

    Article  Google Scholar 

  8. MacDonell MT, Colwell RR (1985) Phylogeny of the Vibrionaceae, and recommendation for two new genera, Listonella and Shewanella. Syst Appl Microbiol 6:171–182. doi:10.1016/S0723-2020(85)80051-5

    Article  CAS  Google Scholar 

  9. Jensen MJ, Tebo BM, Baumann P, Mandel M, Nealson KH (1980) Characterization of Alteromonas hanedai (sp. nov.), a nonfermentative luminous species of marine origin. Curr Microbiol 3:311–315. doi:10.1007/BF02601812

    Article  Google Scholar 

  10. Nogi Y, Kato C, Horikoshi K (1998) Taxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanella violacea sp. nov. Arch Microbiol 170:331–338. doi:10.1007/s002030050650

    Article  CAS  PubMed  Google Scholar 

  11. Ivanova EP, Flavier S, Christen R (2004) Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov. and Psychromonadaceae fam. nov. Int J Syst Evol Microbiol 54:1773–1788. doi:10.1099/ijs.0.02997-0

    Article  CAS  PubMed  Google Scholar 

  12. Bowman JP, McMeekin T (2005) Alteromonadales ord. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, Boone DR, De Vos P, Goodfellow M, Rainey FA, Schleifer KH (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer, US, pp 443–491

    Chapter  Google Scholar 

  13. Janda JM, Abbott SL (2014) The genus Shewanella: from the briny depths below to human pathogen. Crit Rev Microbiol 40:293–312. doi:10.3109/1040841X.2012.726209

    Article  PubMed  Google Scholar 

  14. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49:705–724. doi:10.1099/00207713-49-2-705

    Article  CAS  PubMed  Google Scholar 

  15. Satomi M, Oikawa H, Yano Y (2003) Shewanella marinintestina sp. nov., Shewanella schlegeliana sp. nov. and Shewanella sairae sp. nov., novel eicosapentaenoic-acid-producing marine bacteria isolated from sea-animal intestines. Int J Syst Evol Microbiol 53:491–499. doi:10.1099/ijs.0.02392-0

    Article  CAS  PubMed  Google Scholar 

  16. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128

    Article  CAS  Google Scholar 

  17. Cimmino T, Olaitan AO, Rolain JM (2016) Whole genome sequence to decipher the resistome of Shewanella algae, a multidrug-resistant bacterium responsible for pneumonia, Marseille, France. Expert Rev Anti Infect Ther 14:269–275. doi:10.1586/14787210.2016.1106936

    Article  CAS  PubMed  Google Scholar 

  18. Wang F, Wang J, Jian H, Zhang B, Li S, Wang F, Zeng X, Gao L, Bartlett DH, Yu J, Hu S, Xiao X (2008) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS One 3:e1937. doi:10.1371/journal.pone.0001937

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tena D, Losa C, Carrasco G, Sáez-Nieto JA (2016) Surgical site infection caused by Shewanella putrefaciens: case report and literature review. Infect Dis Clin Pract 24:18–23. doi:10.1097/IPC.0000000000000344

    Article  Google Scholar 

  20. Khashe S, Janda JM (1998) Biochemical and pathogenic properties of Shewanella alga and Shewanella putrefaciens. J Clin Microbiol 36:783–787

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Kueh CS, Kutarski P, Brunton M (1992) Contaminated marine wounds—the risk of acquiring acute bacterial infection from marine recreational beaches. J Appl Bacteriol 73:412–420. doi:10.1111/j.1365-2672.1992.tb04997.x

    Article  CAS  PubMed  Google Scholar 

  22. Byun JH, Park H, Kim S (2016) The phantom menace for the patients with hepatobiliary diseases: Shewanella haliotis, often misidentified as Shewanella algae by biochemical tests and MALDI-TOF. Jpn J Infect Dis. doi:10.7883/yoken.JJID.2015.658

    PubMed  Google Scholar 

  23. Jacob-Kokura S, Chan CY, Kaplan L (2014) Bacteremia and empyema caused by Shewanella algae in a trauma patient. Ann Pharmacother 48:128–136. doi:10.1177/1060028013517630

    Article  PubMed  Google Scholar 

  24. Iwata M, Tateda K, Matsumoto T, Furuya N, Mizuiri S, Yamaguchi K (1999) Primary Shewanella alga septicemia in a patient on hemodialysis. J Clin Microbiol 37:2104–2105

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Tang TH, Cheng NH, Ho RT, Chan HS, Lam KW, Xavier J, Wu TC (2016) Shewanella-related bacteremia and Fournier’s gangrene: a case report. Open Forum Infect Dis 3:ofw148. doi:10.1093/ofid/ofw148

    Article  PubMed  PubMed Central  Google Scholar 

  26. Liu PY, Lin CF, Tung KC, Shyu CL, Wu MJ, Liu JW, Chang CS, Chan KW, Huang JA, Shi ZY (2013) Clinical and microbiological features of Shewanella bacteremia in patients with hepatobiliary disease. Intern Med 52:431–438

    Article  CAS  PubMed  Google Scholar 

  27. Botelho-Nevers E, Gouriet F, Rovery C, Paris P, Roux V, Raoult D, Brouqui P (2005) First case of osteomyelitis due to Shewanella algae. J Clin Microbiol 43:5388–5390. doi:10.1128/JCM.43.10.5388-5390.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Nath R, Saikia L, Choudhury G, Das PP (2011) Isolation of Shewanella algae from rectal swabs of patients with bloody diarrhoea. Indian J Med Microbiol 29:422–425. doi:10.4103/0255-0857.90186

    Article  CAS  PubMed  Google Scholar 

  29. Gautam V, Saigal K, Bhalla A, Ray P (2012) Shewanella algae soft tissue infection in a diabetic patient. J Clin Case Rep 2:234. doi:10.4172/2165-7920.1000234

    Article  Google Scholar 

  30. Tan CK, Lai CC, Kuar WK, Hsueh PR (2008) Purulent pericarditis with greenish pericardial effusion caused by Shewanella algae. J Clin Microbiol 46:2817–2819. doi:10.1128/JCM.01018-08

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gressier M, Mbayo D, Deramond H, Grados F, Eb F, Canarelli B (2010) First case of human spondylodiscitis due to Shewanella algae. Int J Infect Dis 14(Suppl 3):e261–e264. doi:10.1016/j.ijid.2009.11.007

    Article  PubMed  Google Scholar 

  32. Rosenthal SL, Zuger JH, Apollo E (1975) Respiratory colonization with Pseudomonas putrefaciens after near-drowning in salt water. Am J Clin Pathol 64:382–384

    Article  CAS  PubMed  Google Scholar 

  33. Jeffery S (2014) Shewanella dysentery in a patient with underlying malignancy. Med J Malaysia 69:284–285

    CAS  PubMed  Google Scholar 

  34. Chen YS, Liu YC, Yen MY, Wang JH, Wang JH, Wann SR, Cheng DL (1997) Skin and soft-tissue manifestations of Shewanella putrefaciens infection. Clin Infect Dis 25:225–229

    Article  CAS  PubMed  Google Scholar 

  35. Duan M, Wang D, Wang J, Xiao X, Han L, Zhang F (2015) A case report of intracranial infection caused by Shewanella putrefaciens. Neurol Sci 36:625–629. doi:10.1007/s10072-014-1956-5

    Article  PubMed  Google Scholar 

  36. Constant J, Chernev I, Gomez E (2014) Shewanella putrefaciens infective endocarditis. Braz J Infect Dis 18:686–688. doi:10.1016/j.bjid.2014.06.001

    Article  PubMed  Google Scholar 

  37. Holmes B, Lapage SP, Malnick H (1975) Strains of Pseudomonas putrefaciens from clinical material. J Clin Pathol 28:149–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Roger SD, Chen SC, Lawrence S, Sorrell TC (1991) Pseudomonas putrefaciens bacteraemia in a peritoneal dialysis patient. Nephrol Dial Transplant 6:73

    Article  CAS  PubMed  Google Scholar 

  39. Yilmaz G, Aydin K, Bektas D, Caylan R, Caylan R, Koksal I (2007) Cerebellar abscess and meningitis, caused by Shewanella putrefaciens and Klebsiella pneumoniae, associated with chronic otitis media. J Med Microbiol 56:1558–1560. doi:10.1099/jmm.0.47044-0

    Article  PubMed  Google Scholar 

  40. Shimada K, Noro T, Inamatsu T, Urayama K, Adachi K (1981) Bacteriology of acute obstructive suppurative cholangitis of the aged. J Clin Microbiol 14:522–526

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Mohan N, Sharma S, Padhi TR, Basu S, Das TP (2014) Traumatic endophthalmitis caused by Shewanella putrefaciens associated with an open globe fishhook injury. Eye (Lond) 28:235. doi:10.1038/eye.2013.252

    Article  CAS  Google Scholar 

  42. Basir N, Yong AM, Chong VH (2012) Shewanella putrefaciens, a rare cause of splenic abscess. J Microbiol Immunol Infect 45:151–153. doi:10.1016/j.jmii.2011.09.007

    Article  PubMed  Google Scholar 

  43. Yim SY, Kang YS, Cha DR, Park DW, Youn YK, Jo YM, Kim JY, Song JY, Sohn JW, Cheong HJ, Kim WJ, Kim MJ, Choi WS (2010) Fatal PD peritonitis, necrotizing fasciitis, and bacteremia due to Shewanella putrefaciens. Perit Dial Int 30:667–669. doi:10.3747/pdi.2010.00084

    Article  CAS  PubMed  Google Scholar 

  44. Poovorawan K, Chatsuwan T, Lakananurak N, Chansaenroj J, Komolmit P, Poovorawan Y (2013) Shewanella haliotis associated with severe soft tissue infection, Thailand, 2012. Emerg Infect Dis 19:1019–1021. doi:10.3201/eid1906.121607

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zong Z (2011) Nosocomial peripancreatic infection associated with Shewanella xiamenensis. J Med Microbiol 60:1387–1390. doi:10.1099/jmm.0.031625-0

    Article  PubMed  Google Scholar 

  46. Antonelli A, Di Palo DM, Galano A, Becciani S, Montagnani C, Pecile P, Galli L, Rossolini GM (2015) Intestinal carriage of Shewanella xiamenensis simulating carriage of OXA-48-producing Enterobacteriaceae. Diagn Microbiol Infect Dis 82:1–3. doi:10.1016/j.diagmicrobio.2015.02.008

    Article  CAS  PubMed  Google Scholar 

  47. Vignier N, Barreau M, Olive C, Baubion E, Théodose R, Hochedez P, Cabié A (2013) Human infection with Shewanella putrefaciens and S. algae: report of 16 cases in Martinique and review of the literature. Am J Trop Med Hyg 89:151–156. doi:10.4269/ajtmh.13-0055

    Article  PubMed  PubMed Central  Google Scholar 

  48. Brink AJ, van Straten A, van Rensburg AJ (1995) Shewanella (Pseudomonas) putrefaciens bacteremia. Clin Infect Dis 20:1327–1332

    Article  CAS  PubMed  Google Scholar 

  49. Vogel BF, Holt HM, Gerner-Smidt P, Bundvad A, Søgaard P, Gram L (2000) Homogeneity of Danish environmental and clinical isolates of Shewanella algae. Appl Environ Microb 66:443–448

    Article  CAS  Google Scholar 

  50. Holt HM, Gahrn-Hansen B, Bruun B (2005) Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics. Clin Microbiol Infect 11:347–352

    Article  CAS  PubMed  Google Scholar 

  51. Liu PY, Shi ZY, Lin CF, Huang JA, Liu JW, Chan KW, Tung KC (2012) Shewanella infection of snake bites: a twelve-year retrospective study. Clinics (Sao Paulo) 67:431–435. doi:10.6061/clinics/2012(05)05

    Article  Google Scholar 

  52. Liu PY, Shi ZY, Shyu CL, Wu ZY, Lai KL, Chang CY, Chen YJ, Huang JA, Mao YC, Tung KC (2014) Cobra bite wound infection caused by Shewanella algae. Int J Infect Dis 20:11–12. doi:10.1016/j.ijid.2013.08.014

    Article  CAS  PubMed  Google Scholar 

  53. Cai J, Chen H, Thompson KD, Li C (2006) Isolation and identification of Shewanella alga and its pathogenic effects on post-larvae of abalone Haliotis diversicolor supertexta. J Fish Dis 29:505–508. doi:10.1111/j.1365-2761.2006.00732.x

    Article  CAS  PubMed  Google Scholar 

  54. Li H, Qiao G, Li Q, Zhou W, Won KM, Xu DH, Park SI (2010) Biological characteristics and pathogenicity of a highly pathogenic Shewanella marisflavi infecting sea cucumber, Apostichopus japonicus. J Fish Dis 33:865–877. doi:10.1111/j.1365-2761.2010.01189.x

    Article  CAS  PubMed  Google Scholar 

  55. Gram L (1994) Siderophore-mediated iron sequestering by Shewanella putrefaciens. Appl Environ Microbiol 60:2132–2136

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Simidu U, Noguchi T, Hwang DF, Shida Y, Hashimoto K (1987) Marine bacteria which produce tetrodotoxin. Appl Environ Microbiol 53:1714–1715

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Holt HM (2004) Shewanella species: infections in Denmark and phenotypic characterisation. In: Proceedings of the 14th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID), Prague, Czech Republic, May 2004

  58. Kang CH, So JS (2016) Antibiotic and heavy metal resistance in Shewanella putrefaciens strains isolated from shellfishes collected from West Sea, Korea. Mar Pollut Bull 112:111–116. doi:10.1016/j.marpolbul.2016.08.033

    Article  CAS  PubMed  Google Scholar 

  59. Gao T, Ju L, Yin J, Gao H (2015) Positive regulation of the Shewanella oneidensis OmpS38, a major porin facilitating anaerobic respiration, by Crp and Fur. Sci Rep 5:14263. doi:10.1038/srep14263

    Article  PubMed  PubMed Central  Google Scholar 

  60. Héritier C, Poirel L, Nordmann P (2004) Genetic and biochemical characterization of a chromosome-encoded carbapenem-hydrolyzing ambler class D beta-lactamase from Shewanella algae. Antimicrob Agents Chemother 48:1670–1675

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kim HB, Park CH, Gavin M, Jacoby GA, Hooper DC (2011) Cold shock induces qnrA expression in Shewanella algae. Antimicrob Agents Chemother 55:414–416. doi:10.1128/AAC.00991-10

    Article  CAS  PubMed  Google Scholar 

  62. Poirel L, Rodriguez-Martinez JM, Mammeri H, Liard A, Nordmann P (2005) Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob Agents Chemother 49:3523–3525. doi:10.1128/AAC.49.8.3523-3525.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Soledad Ramírez M, Merkier AK, Almuzara M, Vay C, Centrón D (2010) Reservoir of antimicrobial resistance determinants associated with horizontal gene transfer in clinical isolates of the genus Shewanella. Antimicrob Agents Chemother 54:4516–4517. doi:10.1128/AAC.00570-10

    Article  PubMed  PubMed Central  Google Scholar 

  64. Telke AA, Rolain JM (2015) Functional genomics to discover antibiotic resistance genes: The paradigm of resistance to colistin mediated by ethanolamine phosphotransferase in Shewanella algae MARS 14. Int J Antimicrob Agents 46:648–652. doi:10.1016/j.ijantimicag.2015.09.001

    Article  CAS  PubMed  Google Scholar 

  65. Poirel L, Héritier C, Nordmann P (2005) Genetic and biochemical characterization of the chromosome-encoded class B beta-lactamases from Shewanella livingstonensis (SLB-1) and Shewanella frigidimarina (SFB-1). J Antimicrob Chemother 55:680–685. doi:10.1093/jac/dki065

    Article  CAS  PubMed  Google Scholar 

  66. Tacão M, Correia A, Henriques I (2013) Environmental Shewanella xiamenensis strains that carry bla OXA-48 or bla OXA-204 genes: additional proof for blaOXA-48-like gene origin. Antimicrob Agents Chemother 57:6399–6400. doi:10.1128/AAC.00771-13

    Article  PubMed  PubMed Central  Google Scholar 

  67. Ceccarelli D, van Essen-Zandbergen A, Veldman KT, Tafro N, Haenen O, Mevius DJ (2017) Chromosome-based bla OXA-48-like variants in Shewanella species isolates from food-producing animals, fish, and the aquatic environment. Antimicrob Agents Chemother 61(2):e01013-16

    PubMed  PubMed Central  Google Scholar 

  68. Zong Z (2012) Discovery of bla OXA-199, a chromosome-based bla OXA-48-like variant, in Shewanella xiamenensis. PLoS One 7:e48280. doi:10.1371/journal.pone.0048280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhao JY, Mu XD, Zhu YQ, Xi L, Xiao Z (2015) Identification of an integron containing the quinolone resistance gene qnrA1 in Shewanella xiamenensis. FEMS Microbiol Lett 362:fnv146. doi: 10.1093/femsle/fnv146

    Article  PubMed  Google Scholar 

  70. Drouin F, Mélançon J, Roy PH (2002) The IntI-like tyrosine recombinase of Shewanella oneidensis is active as an integron integrase. J Bacteriol 184:1811–1815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Zhou Y, Ng IS (2016) Explored a cryptic plasmid pSXM33 from Shewanella xiamenensis BC01 and construction as the shuttle vector. Biotechnol Bioprocess Eng 21:68–78. doi:10.1007/s12257-015-0618-7

    Article  CAS  Google Scholar 

  72. Pembroke JT, Piterina AV (2006) A novel ICE in the genome of Shewanella putrefaciens W3-18-1: comparison with the SXT/R391 ICE-like elements. FEMS Microbiol Lett 264:80–88. doi:10.1111/j.1574-6968.2006.00452.x

    Article  CAS  PubMed  Google Scholar 

  73. Rodríguez-Blanco A, Lemos ML, Osorio CR (2012) Integrating conjugative elements as vectors of antibiotic, mercury, and quaternary ammonium compound resistance in marine aquaculture environments. Antimicrob Agents Chemother 56:2619–2626

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Touati.

Ethics declarations

Not applicable.

Conflict of interest

None to declare.

Funding

None to declare

Ethical approval

Not applicable.

Informed consent

Not applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yousfi, K., Bekal, S., Usongo, V. et al. Current trends of human infections and antibiotic resistance of the genus Shewanella . Eur J Clin Microbiol Infect Dis 36, 1353–1362 (2017). https://doi.org/10.1007/s10096-017-2962-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-017-2962-3

Keywords

Navigation