Prevalence and genetic variability of Plesiomonas shigelloides in temperate climate surface waters of the Pannonian Plain
Keywords:
Plesiomonas shigelloides, surface waters, temperate climate, isolation, RAPD-PCRAbstract
Plesiomonas shigelloides, a Gram-negative bacterium and the causative agent of intestinal diseases and extraintestinal infections in humans and animals, is most frequently found in aquatic environments in tropical or subtropical areas. The present study was designed to establish the prevalence and genetic variability of P. shigelloides in surface waters (lakes, rivers, ponds, inlets and canals) located in a temperate climate zone, namely the Pannonian Plain of the northern part of Serbia and southern part of Hungary. The strains were isolated directly by plating samples on inositol-brilliant green-bile agar with neutral red or phenol red as indicators. Our results indicate that phenol red effectively facilitates differentiation of P. shigelloides from other bacteria. A number of samples were enriched using alkaline peptone water broth, peptone inositol-bile broth and tetrathionate broth. The recovery of the isolates was more successful with the first medium. Out of a total of 51 water samples collected from 28 different locations, 22 samples (43.1%) were found positive for P. shigelloides. Among the 37 isolated strains, 34 were from lakes (Šatrinci, Ludaš, Panonija, Krivaja, Pecs, Kapetanski rit, Pavlovci, Kovácsszénája, Dobrodol, Vranjaš, Borkovac, Hermann Ottó, Sot, Šelevrenac, Zobnatica, Palić, Orfüí, Jarkovci, Čonoplja) and 3 were from rivers (Danube, Sava). The strains were identified by phenotypic characteristic or by the VITEK2 system and confirmed by PCR using 23S rRNA species-specific oligos. The strains showed a high genetic variability, displaying a variety of RAPD profiles. Our results reveal for the first time a high prevalence of genetically diverse P. shigelloides populations in surface waters located in the temperate climate of central and southeastern Europe.
https://doi.org/10.2298/ABS170530029P
Received: May 30, 2017; Revised: July 17, 2017; Accepted: July 26, 2017; Published online: August 24, 2017
How to cite this article: Petrušić M, Obreht Vidaković D, Lazić S, Radnović D, Knežević P. Prevalence and genetic variability of Plesiomonas shigelloides in temperate climate surface waters of the Pannonian Plain. Arch Biol Sci. 2018;70(1):99-108.
Downloads
References
Arai T, Ikejima N, Itoh T, Sakai S, Shimada T, Sakazaki R. A survey of Plesiomonas shigelloides from aquatic environments, domestic animals, pets and humans. J Hyg. 1980;84(02):203-11.
Mondino S, Nunes M, Ricciardi I. Occurrence of Plesiomonas shigelloides in water environments of Rio de Janeiro city. Mem I Oswaldo Cruz. 1995;90(1):1-4.
Aldova E, Melter O, Chyle P, Slorasek M, Kodym, P. Plesiomonas shigelloides in water and fish. Cent Eur J Publ Health. 1999;7:172-5.
Krovacek K, Eriksson L, González-Rey C, Rosinsky J, Ciznar I. Isolation, biochemical and serological characterisation of Plesiomonas shigelloides from freshwater in Northern Europe. Comp Immunol Microb. 2000;23(1):45-51.
Matsuyama R, Kuninaga N, Morimoto T, Shibano T, Sudo A, Sudo K, Asano M, Suzuki M, Asai T. Isolation and antimicrobial susceptibility of Plesiomonas shigelloides from great cormorants (Phalacrocorax carbo hanedae) in Gifu and Shiga prefectures, Japan. J Vet Med Sci. 2015;77:1179-81.
Janda, J. Family I. Enterobacteriaceae, genus XXVII. Plesiomonas Habs and Schubert 1962. In: Brenner D, Krieg NR, Staley JT, editors. Bergey's manual of systematic bacteriology. Vol. 2. 2nd ed. New York: Springer; 2005. p 740-4.
Rouf M, Rigney M. Growth Temperatures and Temperature Characteristics of Aeromonas. Appl Microbiol. 1971;22(4):503-6.
Miller M, Koburger J. Tolerance of Plesiomonas shigelloides to pH, Sodium Chloride and Temperature. J Food Protect. 1986;49(11):877-9.
Ferguson W, Henderson N. Description of Strain C27: A Motile Organism with the Major Antigen of Shigella sonnei Phase I. J Bacteriol. 1947;54(2):179-81.
Koburger, J. Plesiomonas shigelloides. In: Doyle M, editor. Foodborne Bacterial Pathogens. New York: Marcel Dekker; 1989. p. 311-26.
Hendrie M, Shewan J, Veron M. Aeromonas shigelloides (Bader) Ewing et al: A proposal that it be transferred to the genus Vibrio. Int J Sys Bacteriol. 1971;21:25-7.
MacDonell M, Swartz D, Ortiz-Conde B, Last G, Colwell R. Ribosomal RNA phylogenies for the vibrio-enteric group of eubacteria. Microbiol Sci. 1986;3:172-8.
East A, Allaway D, Collins M. Analysis of DNA encoding 23S rRNA and 16S-23S rRNA intergenic spacer regions from Plesiomonas shigelloides. FEMS Microbiol Lett. 1992;95(1):57-62.
Martinez-Murcia A, Benlloch S, Collins M. Phylogenetic Interrelationships of Members of the Genera Aeromonas and Plesiomonas as Determined by 16S Ribosomal DNA Sequencing: Lack of Congruence with Results of DNA-DNA Hybridizations. Int J Syst Bacteriol. 1992;42(3):412-21.
Ruimy R, Breittmayer V, Elbaze P, Lafay B, Boussemart O, Gauthier M, Christen R. Phylogenetic Analysis and Assessment of the Genera Vibrio, Photobacterium, Aeromonas, and Plesiomonas Deduced from Small-Subunit rRNA Sequences. Int J Syst Bacteriol. 1994;44(3):416-26.
Van Damme L, Vanderpille J. Frequent isolation of Edwardsiella tarda and Plesiomonas shigelloides from healthy Zairese freshwater fish; A possible source of sporadic diarrhea in the tropics. Appl Environ Microbiol. 1980;39:475-79.
Islam M, Alam M, Khan S. Distribution of Plesiomonas shigelloides in Various Components of Pond Ecosystems in Dhaka, Bangladesh. Microbiol Immunol. 1991;35(11):927-32.
Obi C, Coker A, Epoke J, Ndip R. Aeromonas and Plesiomonas species as bacterial agents of diarrhoea in urban and rural areas of Nigeria: antibiogram of isolates. Cent Afr J Med. 1995;41(12):397-403.
Shigematsu M, Kaufmann M, Charlett A, Niho Y, Pitt T. An epidemiological study of Plesiomonas shigelloides diarrhoea among Japanese travellers. Epidemiology and Infection. 2000;125(3):523-30.
Wong T, Tsui H, So M, Lai J, Lai S, Tse C, Ng T. Plesiomonas shigelloides infection in Hong Kong: retrospective study of 167 laboratory-confirmed cases. Hong Kong Med J. 2000;6(4):375-80.
Tseng H, Liu C, Li W, Su S, Lee C. Characteristics of Plesiomonas shigelloides infection in Taiwan. J Microbiol Immunol Infect. 2002;35:47-52.
Maluping R, Lavilla-Pitogo C, DePaola A, Janda J, Krovacek K, Greko C. Antimicrobial susceptibility of Aeromonas spp., Vibrio spp. and Plesiomonas shigelloides isolated in the Philippines and Thailand. Int J Antimicrob Ag. 2005;25(4):348-50.
Chen X, Chen Y, Yang Q, Kong H, Yu F, Han D, Zheng S, Cui D, Li L. Plesiomonas shigelloides Infection in Southeast China. PLoS ONE. 2013;8(11):e77877.
Kwaga J, Adesiyun A, Bello C, Abdullahi S. Occurrence of Plesiomonas shigelloides in humans and water in Zaria, Nigeria. Microbiologica 1988;11:165-67.
Canosa A, Pinilla G. Bacteriological eutrophication indicators in four Colombian water bodies (South America). Lakes Reservoirs: Res Manage. 1999;4(1):23-7.
Gibotti A, Saridakis H, Pelayo J, Tagliari K, Falcao D. Prevalence and virulence properties of Vibrio cholerae non-O1, Aeromonas spp. and Plesiomonas shigelloides isolated from Cambe Stream (State of Parana, Brazil). J Appl Microbiol. 2000;89(1):70-5.
Medema G, Schets C. Occurrence of Plesiomonas shigelloides in surface water: relationship with faecal pollution and trophic state. Zentralbl Hyg. 1993;194:398-404.
Bardon J, Plesiomonas shigelloides and its serovars in animals in the Czech Republic – Region Moravia. Cent Eur J Publ Heal. 1999;1:47-9.
Gonzalez-Rey C, Svenson S, Eriksson L, Ciznar I, Krovacek K. Unexpected finding of the "tropical" bacterial pathogen Plesiomonas shigelloides from lake water north of the Polar Circle. Polar Biol. 2003;26(8):495-9.
Reinhardt J, George W. Plesiomonas shigelloides-associated diarrhea. JAMA- J Am Med Assoc. 1985;253(22):3294-5.
Holmberg S, Farmer J. Aeromonas hydrophila and Plesiomonas shigelloides as Causes of Intestinal Infections. Clin Infect Dis. 1984;6(5):633-9.
Holmberg S, Wachsmuth I, Hickman-Brenner F, Blake P, Farmer J. Plesiomonas Enteric Infections in the United States. Ann Inter Med. 1986;105(5):690.
Murray P, Baron E, Jorgensen J, Landry M, Pfaller M, Yolken R. Manual of Clinical Microbiology. 8th ed. Herdon, VA, USA: American Society for Microbiology; 2003.
Rutala W, Sarubbi F, Finch C, Maccormack J, Steinkraus G. Oyster-associated outbreak of diarrhoeal disease possibly caused by Plesiomonas shigelloides. Lancet. 1982;319(8274):739.
Kain K, Kelly M. Clinical features, epidemiology, and treatment of Plesiomonas shigelloides diarrhea. J Clin Microbiol. 1989;27(5):998-1001.
Bhat P, Shanthakumari S, Rajan D. The characterization and significance of Plesiomonas shigelloides and Aeromonas hydrophila isolated from an epidemic of diarrhoea. Indian J Med Res. 1974;62(7):1051-60.
Vandepitte J, Makulu A, Gatti F. Plesiomonas shigelloides Survey and possible association with diarrhoea in Zaire. Ann Soc Belg Med Trop. 1974;54(6):503-13.
Bodhidatta L, Serichantalergs O, Sornsakrin S, McDaniel P, Mason C, Srijan A. Case-Control Study of Diarrheal Disease Etiology in a Remote Rural Area in Western Thailand. Am J Trop Med Hyg. 2010;83(5):1106-9.
Escobar J, Bhavnani D, Trueba G, Ponce K, Cevallos W, Eisenberg J. Plesiomonas shigelloides Infection, Ecuador, 2004–2008. Emerg Infect Dis. 2012;18(2):322-4.
Ingram C, Morrison A, Levitz R. Gastroenteritis, sepsis, and osteomyelitis caused by Plesiomonas shigelloides in an immunocompetent host: case report and review of the literature. J Clin Microbiol. 1987;25(9):1791-3.
Paul R, Siitonen A, Kärkkäinen P. Plesiomonas shigelloides bacteremia in a healthy girl with mild gastroenteritis, J Clin Microbiol. 1990;28:1445-6.
Brenden R, Miller M, Janda J. Clinical Disease Spectrum and Pathogenic Factors Associated with Plesiomonas shigelloides Infections in Humans. Clin Infect Dis. 1988;10(2):303-16.
Rolston K, Hopper R. Diarrhoea due to Plesiomonas shigelloides to cancer patients. J Clin Microbiol. 1984;20:597-8.
Austin B, Austin D. Bacterial fish pathogens. 4th ed. Chichester: Springer; 2007.
Cruz J, Saraiva A, Eiras J, Branco R, Sousa J. An outbreak of Plesiomonas shigelloides in farmed rainbow trout, Salmo gairdneri Richardson, in Portugal. B Eur Assoc Fish Pat. 1986;8(1):20-2.
Klein B, Kleingeld D, Bohm K. First isolations of Plesiomonas shigelloides from samples of cultured fish in Germany. B Eur Assoc Fish Pat. 1993;13:70-2.
Miller M, Koburger J. Plesiomonas shigelloides: An Opportunistic Food and Waterborne Pathogen. J Food Protect. 1985;48(5):449-57.
Claesson B, Holmlund D, Lindhagen C, Mätzsch T. Plesiomonas shigelloides in acute cholecystitis: a case report. J Clin Microbiol. 1984;20:985-7.
Van Houten R, Farberman D, Norton J, Ellison J, Kiehlbauch J, Morris T, Smith P. Plesiomonas shigelloides and Salmonella serotype Hartford infections associated with a contaminated water supply—Livingston County, New York, 1996. Morb Mortal Wkly Rep. 1998;47:394-6.
Monge R, Arias-Echandi M, Utzinger D. Presence of cytotoxic Aeromonas and Plesiomonas shigelloides in fresh vegetables. Rev Biomed. 1998;9:176-80.
Jagger TD. Plesiomonas shigelloides: a veterinary perspective. Infect Dis Rev. 2000;2:199–210.
Freund S, Koburger J, Wei C. Enhanced Recovery of Plesiomonas shigelloides following an Enrichment Technique. J Food Protect. 1988;51(2):110-2.
González-Rey C, Svenson S, Bravo L, Rosinsky J, Ciznar I, Krovacek K. Specific detection of Plesiomonas shigelloides isolated from aquatic environments, animals and human diarrhoeal cases by PCR based on 23S rRNA gene. FEMS Immunol Med Microbiol. 2000;29(2):107-13.
Garcia-Vallve S, Palau J, Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol Biol Evol. 1999;16(9):1125-34.
DendroUPGMA: A dendrogram construction utility. [Internet]. Tarragona (Spain): Universitat Rovira i Virgili (URV); 2002 [cited 2017 Mar 1]. Available from: http://genomes.urv.cat/UPGMA/index.php
Stöver B, Müller K. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics. 2010;11:7.
Penn R, Giber D, Knoop F, Preheim L. Plesiomonas shigelloides overgrowth in the small intestine. J Clin Microbiol. 1982;15:869-72.
Pitarangsi C, Echeverria P, Whitmire R, Tirapat C, Formal S, Dammin GJ, Tingtalapong M. Enteropathogenicity of Aeromonas hydrophila and Plesiomonas shigelloides: prevalence among individuals with and without diarrhea in Thailand. Infect Immun. 1982;35(2):666-73.
Huq M, Islam M. Microbiological and clinical studies in diarrhoea due to Plesiomonas shigelloides. Indian J Med Res. 1983;77:793-7.
Tsukamoto T, Kinoshita Y, Shimada T, Sakazaki R. Two epidemics of diarrhoeal disease possibly caused by Plesiomonas shigelloides. J Hyg. 1978;80(02):275-80.
Sakazaki R, Balows A. The genera Vibrio, Plesiomonas, and Aeromonas. In: Starr M, Stolp H, Trüper H, Balows A, Schlegel H, editors. A handbook on habitats, isolation and identification of bacteria. Berlin: Springer-Verlag; 1981. p. 1284-1301.
Schubert R. Ueber den Nachweis von Plesiomonas shigelloides Habs und Schubert. 1962, und ein Elektivmedium, den Inositol-Brillantgrun-Gallesalz-Agar. Emst-Rodenwaldt-Arch. 1977;4:97-103.
Gu W, Gonzalez-Rey C, Krovacek K, Levin R. Genetic Variability Among Isolates of Plesiomonas shigelloides from Fish, Human Clinical Sources and Fresh Water, Determined by RAPD Typing. Food Biotechnol. 2006;20(1):1-12.
González-Rey C, Siitonen A, Pavlova A, Ciznar I, Svenson S, Krovacek K. Molecular evidence of Plesiomonas shigelloides as a possible zoonotic agent. Folia Microbiol. 2011;56(2):178-84.
Salerno A, Deletoile A, Lefevre M, Ciznar I, Krovacek K, Grimont P, Brisse, S. Recombining Population Structure of Plesiomonas shigelloides (Enterobacteriaceae) Revealed by Multilocus Sequence Typing. J Bacteriol. 2007;189(21):7808-18.
Selander R, Levin B. Genetic diversity and structure in Escherichia coli populations. Science. 1980;210(4469):545-7.
Beltran P, Musser J, Helmuth R, Farmer J, Frerichs W, Wachsmuth I, Ferris K, McWhorter A, Wells J, Cravioto A. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A. 1988;85(20):7753-7.
Dolina M, Peduzzi R. Population genetics of human, animal, and environmental Yersinia strains. Appl Environ Microb. 1993;59(2):442-50.
Downloads
Published
How to Cite
Issue
Section
License
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.
