Abstract
Despites Providencia heimbachae has been isolated from human, penguin, and bovine fetus, relatively little information is available regarding the pathogenicity and biologic characteristics of P. heimbachae. Here, we report that investigation of post-weaning diarrhea yielded bacterial isolates identified as P. heimbachae based on the biochemical tests and 16S ribosomal DNA sequence analysis. The two isolates were positive for utilization of Malonate, no gas production from glucose, and non-fermentation of D-mannitol, D-Galactose, and L-Rhamnose that were different from those of the type strain, and both of them have the ability of adhesion and invasion to IPEC-J2 cells, and were resistant to 21 out of the 41 antibiotics tested. In addition, the isolate 99101 was highly pathogenic to mice and piglets. Histopathology studies on nerve tissue of piglets that developed hindlimb paralysis showed microglia cell infiltration and neuron damage in the spinal cord. Notably, the strains could grow under low temperature (4 °C), which raise attention of a new risk factor for food safety. To the best of our knowledge, this is the first report of P. heimbachae strain caused post-weaning diarrhea in piglets in both natural and experimental conditions. These findings extended the knowledge of P. heimbachae as an important zoonotic agent, which should be given more attention during surveillance and diagnostics.
Similar content being viewed by others
Data Availability
The data were deposited in NCBI GenBank (accession numbers for NCBI: GenBank: CP 028384.1 for complete genome of Strain 99101; GenBank: MT 974580 for 16S rRNA sequencing of Strain WY2).
References
Rhouma M, Fairbrother JM, Beaudry F, Letellier A (2017) Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Vet Scand 59(1):31. https://doi.org/10.1186/s13028-017-0299-7
Amezcua R, Friendship RM, Dewey CE, Gyles C, Fairbrother JM (2002) Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns. Can J Vet Res 66(2):73–78. https://doi.org/10.1080/03079450120118685
Fairbrother JM, Nadeau E, Gyles CL (2005) Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev 6(1):17–39. https://doi.org/10.1079/ahr2005105
Jayaraman B, Nyachoti CM (2017) Husbandry practices and gut health outcomes in weaned piglets: a review. Anim Nutr 3(3):205–211. https://doi.org/10.1016/j.aninu.2017.06.002
Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA et al (2009) The NIH human microbiome project. Genome Res 19(12):2317–2323. https://doi.org/10.1101/gr.096651.109
Muller HE, O"Hara CM, Fanning GR, Hickman-Brenner FW, Swenson JM, Brenner DJ, (1986) Providencia heimbachae, a new species of Enterobacteriaceae isolated from animals. Int J Syst Bacteriol 36(2):252–256. https://doi.org/10.1099/00207713-36-2-252
Somvanshi VS, Lang E, Straubler B, Sproer C, Schumann P, Ganguly S, Saxena AK, Stackebrandt E (2006) Providencia vermicola sp. nov., isolated from infective juveniles of the entomopathogenic nematode Steinernema thermophilum. Int J Syst Evol Microbiol 56(3):629–633. https://doi.org/10.1099/ijs.0.63973-0
Yoh M, Matsuyama J, Ohnishi M, Takagi K, Miyagi H, Mori K (2005) Importance of Providencia species as a major cause of travellers’ diarrhoea. J Med Microbiol 54(Pt 11):1077–1082. https://doi.org/10.1099/jmm.0.45846-0
Khunthongpan S, Sumpavapol P, Tanasupawat S, Benjakul S (2013) Providencia thailandensis sp. nov., isolated from seafood processing wastewater. J Gen Appl Microbiol 59(3):185–190. https://doi.org/10.2323/jgam.59.185
Hu Y, Feng Y, Zhang X, Zong Z (2019) Providencia huaxiensis sp. nov., recovered from a human rectal swab. Int J Syst Evol Microbiol 69(9):2638–2643. https://doi.org/10.1099/ijsem.0.003502
Juneja P, Lazzaro BP (2009) Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. Int J Syst Evol Microbiol 59(5):1108–1111. https://doi.org/10.1099/ijs.0.000117-0
Mobley HLT, Chippendale GR, Tenney JH, Warren JW (1986) Adherence to Uroepithelial Cells of Providencia stuartii Isolated from the Catheterized Urinary Tract. J Gen Microbiol 132(10):2863–2872. https://doi.org/10.1099/00221287-132-10-2863
Stickler DJ (2008) Bacterial biofilms in patients with indwelling urinary catheters. Nat Clin Pract Uro 5(11):598–608. https://doi.org/10.1038/ncpuro1231
De Vecchi E, Sitia S, Romano CL, Ricci C, Mattina R, Drago L (2013) Aetiology and antibiotic resistance patterns of urinary tract infections in the elderly: a 6-month study. J Med Microbiol 62(Pt 6):859–863. https://doi.org/10.1099/jmm.0.056945-0
Simon C, Dieli M, Brucato A, Pedrotti P, Ferrazzi P (2010) Images in cardiovascular medicine. Bacterial pericarditis due to Providencia stuartii: an atypical case of relapsing pericarditis. Circulation 122(4):401–403. https://doi.org/10.1161/CIRCULATIONAHA.110.943118
Krake PR, Tandon N (2004) Infective endocarditis due to Providenca stuartii. South Med J 97(10):1022–1023. https://doi.org/10.1097/01.smj.0000141308.19657.ba
Unverdi S, Akay H, Ceri M, Inal S, Altay M, Demiroz AP (2011) Peritonitis due to Providencia stuartii. Perit Dial Int 31(2):216–217. https://doi.org/10.3747/pdi.2010.00172
Sipahi OR, Bardak-Ozcem S, Ozgiray E, Aydemir S, Yurtseven T, Yamazhan T et al (2010) Meningitis due to Providencia stuartii. J Clin Microbiol 48(12):4667–4668. https://doi.org/10.1128/JCM.01349-10
Traub WH, Craddock ME, Raymond EA, Fox M, McCall CE (1971) Characterization of an unusual strain of Proteus rettgeri associated with an outbreak of nosocomial urinary-tract infection. Appl Microbiol 22(3):278–283. https://doi.org/10.1002/jctb.5020220617
Sharma D, Sharma P, Soni P (2017) First case report of Providencia Rettgeri neonatal sepsis. BMC Res Notes 10(1):536. https://doi.org/10.1186/s13104-017-2866-4
Takeshi M, Tetsuya I, Yoshitaka S, Kenichi T, Yukihiro A, Itaru Y (2001) A large outbreak of foodborne infection attributed to Providencia alcalifaciens. J Infect Dis 184(8):1050–1055. https://doi.org/10.1086/323458
Shah MM, Odoyo E, Larson PS, Apondi E, Kathiiko C, Miringu G (2015) First report of a foodborne Providencia alcalifaciens outbreak in Kenya. Am J Trop Med Hyg 93(3):497–500. https://doi.org/10.4269/ajtmh.15-0126
Chlibek R, Jirous J, Beran J (2002) Diarrhea outbreak among Czech army field hospital personnel caused by Providencia alcalifaciens. J Travel Med 9(3):151–152. https://doi.org/10.2310/7060.2002.2319023
Albert MJ, Faruque AS, Mahalanabis D (1998) Association of Providencia alcalifaciens with diarrhea in children. J Clin Microbiol 36(5):1433–1435. https://doi.org/10.1128/JCM.36.5.1433-1435.1998
Guth BEC, Perrella E (1996) Prevalence of invasive ability and other virulence-associated characteristics in Providencia alcalifaciens strains isolated in So Paulo. Brazil J Med Microbiol 45(6):459–462. https://doi.org/10.1099/00222615-45-6-459
Haynes J, Hawkey PM (1989) Providencia alcalifaciens and travellers’ diarrhoea. BMJ 299(6691):94–95. https://doi.org/10.1136/bmj.299.6691.94-a
Janda JM, Abbott SL, Woodward D, Khashe S (1998) Invasion of HEp-2 and other eukaryotic cell lines by Providenciae: further evidence supporting the role of Providencia alcalifaciens in bacterial gastroenteritis. Curr Microbiol 37(3):159–165. https://doi.org/10.1007/s002849900357
Möhr AJ, Merwe L, Lugt J, Josling D, Picard J (2002) Primary bacterial enteritis caused by Providencia alcalifaciens in three dogs. Vet Rec 150(2):52–53. https://doi.org/10.1136/vr.150.2.52
Papadogiannakis E, Perimeni D, Velonakis E, Kontos V, Vatopoulos AJ (2010) Providencia stuartii infection in a dog with severe skin ulceration and cellulitis. J Small Anim Pract 48(6):343–345. https://doi.org/10.1128/JCM.37.9.3048-3050.1999
Janda JM, Abbott SL (2006) The enterobacteria, 92nd edn. American Society for Microbiology, Washington, pp 137–150
Camus AC, Hawke JP (2002) Providencia rettgeri-associated Septicemia and Meningoencephalitis in Juvenile Farmed American Alligators Alligator mississippiensis. J Aquat Anim Health 14(2):149–153. https://doi.org/10.1577/1548-8667(2002)0142.0.CO;2
Ladds PW, Bradley J, Hirst RG (1996) Providencia rettgeri meningitis in hatchling saltwater crocodiles (Crocodylus porosus). Aust Vet J 74(5):397–398. https://doi.org/10.1111/j.1751-0813.1996.tb15456.x
Wang XL, Wang JQ, Hao HF, Qiu L, Liu HJ, Chen SL (2014) Pathogenic Providencia alcalifaciens strain that causes fatal hemorrhagic pneumonia in piglets. Curr Microbiol 68(3):278–284. https://doi.org/10.1007/s00284-013-0470-y
Kycko A, Kozaczynski W, Jasik A, Kedrak-Jablonska A, Borkowska-Opacka B, Reichert M (2013) Granulomatous pneumonia and hepatitis associated with Providencia rettgeri infection in a crocodile monitor lizard (Varanus salvadorii). Acta Vet Hung 61(1):51–58. https://doi.org/10.1556/AVet.2012.052
Chander Y, Goyal SM, Gupta SC (2006) Antimicrobial resistance of Providencia spp. isolated from animal manure. Vet J 172(1):188–191. https://doi.org/10.1016/j.tvjl.2005.01.004
Aubert D, Naas T, Lartigue MF, Nordmann P (2005) Novel genetic structure associated with an extended-spectrum β-lactamase blaVEB gene in a Providencia stuartii clinical isolate from Algeria. Antimicrob Agents Chemother 49(8):3590–3592. https://doi.org/10.1128/AAC.49.8.3590-3592.2005
O’Hara CM, Brenner FW, Miller JM (2000) Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev 13(4):534–546. https://doi.org/10.1128/cmr.13.4.534-546.2000
Moyer CL (1994) Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi Seamount. Hawaii Appl Environ Microbiol 60(3):871–879. https://doi.org/10.1128/AEM.60.3.871-879.1994
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Di H, Liang S, Li Q et al (2018) Providencia in retail meats from Guangzhou, China and Osaka, Japan: prevalence, antimicrobial resistance and characterization of classes 1, 2 and 3 integrons. J Vet Med Sci 80(5):829–835. https://doi.org/10.1292/jvms.18-0037
Yan X, Gu S, Shi Y, Cui X, Wen S, Ge J (2017) The effect of emodin on Staphylococcus aureus strains in planktonic form and biofilm formation in vitro. Arch Microbiol 199(9):1267–1275. https://doi.org/10.1007/s00203-017-1396-8
Adolph S, Fuhrmann H, Schumann J (2012) Unsaturated fatty acids promote the phagocytosis of P. aeruginosa and R. equi by RAW264.7 macrophages. Curr Microbiol 65(6):649–655. https://doi.org/10.1007/s00284-012-0207-3
Shu-I TU, Patterson D, Uknalis J (2010) Adenosine triphosphate enhances the fluorescence of 4’,6-diamidino-2-phenylindole (DAPI)-labeled Escherichia coli O157:H71. J Food Saf 18(2):113–126. https://doi.org/10.1111/j.1745-4565.1998.tb00207.x
Tareb R, Bernardeau M, Gueguen M, Vernoux JP (2013) In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol 62(4):637–649. https://doi.org/10.1099/jmm.0.049965-0
Diomande SE, Chamot S, Antolinos V, Vasai F, Guinebretiere MH, Bornard I et al (2014) The CasKR two-component system is required for the growth of mesophilic and psychrotolerant Bacillus cereus strains at low temperatures. Appl Environ Microbiol 80(8):2493–2503. https://doi.org/10.1128/Aem.00090-14
Veen JVD, Nunen MC (1964) Examination for infection with Mycoplasma pneumoniae (Eaton agent). Antonie Van Leeuwenhoek 30(1):111–111. https://doi.org/10.1007/BF02046711
O’Hara CM, Steigerwalt AG, Green D, Mcdowell M, Miller JM (1999) Isolation of Providencia heimbachae from human feces. J Clin Microbiol 37(9):3048–3050. https://doi.org/10.1128/JCM.37.9.3048-3050.1999
Davies J (1996) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417–433. https://doi.org/10.1128/MMBR.00016-10
Khashe S, Scales DJ, Abbott SL, Janda JMJCM (2002) Non-invasive Providencia alcalifaciens strains fail to attach to HEp-2 cells. Curr Microbiol 43(6):414–417
Soultos N, Abrahim A, Papageorgiou K, Steris V (2007) Incidence of Listeria spp in fish and environment of fish markets in Northern Greece. Food Control. https://doi.org/10.1016/j.foodcont.2006.01.006
Imran M, Desmasures N, Coton M, Coton E, Le Fleche-Mateos A, Irlinger F et al (2019) Safety assessment of Gram-negative bacteria associated with traditional French cheeses. Food Microbiol 79:1–10. https://doi.org/10.1016/j.fm.2018.11.001
Albert MJ, Alam K, Ansaruzzaman M, Islam MM, Rahman AS, Haider K et al (1992) Pathogenesis of Providencia alcalifaciens-induced diarrhea. Infect Immun 60(12):5017–5024. https://doi.org/10.1128/IAI.60.12.5017-5024.1992
Acknowledgements
We thank Dr. Dexing Ma at Northeast Agricultural University and Dr. Sen Hu at Harbin Veterinary Research Institute for critically reading the manuscript. We thank Dr. Ping Zhang for technical support.
Funding
This work was financially supported by National Natural Science Foundation of China (Grant No. 31672532), the Natural Science Foundation of Heilongjiang Province (LC2015006) and the SIPT program of Northeast Agricultural University (202010224006). This work was partially supported by the Project (SKLVEB2018KFKT012) from the State Key Laboratory of Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences.
Author information
Authors and Affiliations
Contributions
JG, and HC conceived and designed the work. JG, LZ, and HC coordinated technical support and funding. ZZ wrote the manuscript. ZZ, LZ, MS, HL, KX and CH performed the experiments and collected the samples. ZZ acquired, analyzed, and interpreted the data. JG reviewed the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare there are no conflicts of interest.
Ethical Approval
The experimental protocol was accepted by the international recommendations for animal welfare and the Ethical Committee for animal sciences of Heilongjiang province. The animal Ethics Committee approval number is SYXK(Hei)2017-009.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, Z., Zhao, L., Song, M. et al. Providencia heimbachae Associated with Post-weaning Diarrhea in Piglets: Identification, Phenotype, and Pathogenesis. Curr Microbiol 79, 1 (2022). https://doi.org/10.1007/s00284-021-02697-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-021-02697-1