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Applied and Environmental Microbiology, July 2002, p. 3462-3466, Vol. 68, No. 7
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.7.3462-3466.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Klebsiella pneumoniae Produces No Histamine: Raoultella planticola and Raoultella ornithinolytica Strains Are Histamine Producers

Masashi Kanki,^* Tomoko Yoda, Teizo Tsukamoto, and Tadayoshi Shibata

Osaka Prefectural Institute of Public Health, Higashinari-ku, Osaka 537-0025, Japan

Received 11 December 2001/ Accepted 11 April 2002

Top Abstract Introduction Materials and Methods Results Discussion References

 
Histamine fish poisoning is caused by histamine-producing bacteria (HPB). Klebsiella pneumoniae and Klebsiella oxytoca are the best-known HPB in fish. However, 22 strains of HPB from fish first identified as K. pneumoniae or K. oxytoca by commercialized systems were later correctly identified as Raoultella planticola (formerly Klebsiella planticola) by additional tests. Similarly, five strains of Raoultella ornithinolytica (formerly Klebsiella ornithinolytica) were isolated from fish as new HPB. R. planticola and R. ornithinolytica strains were equal in their histamine-producing capabilities and were determined to possess the hdc genes, encoding histidine decarboxylase. On the other hand, a collection of 61 strains of K. pneumoniae and 18 strains of K. oxytoca produced no histamine.

Top Abstract Introduction Materials and Methods Results Discussion References

 
Histamine fish poisoning (HFP) caused by eating spoiled fish happens throughout the world (2, 3). HFP is usually a rather mild illness; however, serious complications, such as cardiac and respiratory manifestations, occur rarely in individuals with preexisting conditions (12). The implicated fish are mainly of the families Scomberesocidae and Scombridae (the so-called scombroid fish) and contain large amounts of histamine (21). A hazardous level of histamine is produced by the microbial decarboxylation of the free histidine in the muscular tissue of fish. Enteric bacteria have been reported to be the dominant histamine-producing bacteria (HPB) in fish (19). In 1979, Taylor et al. reported that histamine-producing Klebsiella pneumoniae strain T2 was isolated from spoiled tuna sashimi (20). K. pneumoniae has been the best-known HPB ever since that report, and Klebsiella oxytoca is also known as an HPB from fish (13). However, K. pneumoniae strain T2 was later sent to the American Type Culture Collection (now in Manassas, Va.) and identified as Klebsiella planticola (ATCC 43176) in 1987. This strain has been reported to possess the hdc genes, encoding pyridoxal phosphate-dependent histidine decarboxylase (8).

In 1981, Bagley et al. proposed the name Klebsiella planticola for "Klebsiella species 2" to distinguish it from both K. pneumoniae and K. oxytoca (1). Moreover, K. planticola, together with Klebsiella ornithinolytica and Klebsiella terrigena, was classified in the new genus Raoultella in 2001 (5). Nevertheless, Raoultella planticola cannot be distinguished from K. pneumoniae or K. oxytoca by using commercialized systems, such as API 20E (Biomérieux, Marcy l'Etoile, France). Additional tests are necessary to differentiate R. planticola from Klebsiella species (14, 15). Similarly, in 1989 the name Klebsiella ornithinolytica was proposed for "NIH group 12" at the National Institute of Health, Tokyo, Japan, and "Klebsiella group 47" at the Centers for Disease Control, Atlanta, Ga., which showed positive reactions in indole production and ornithine decarboxylase tests (6, 18). K. ornithinolytica was also classified in the genus Raoultella.

K. pneumoniae and K. oxytoca had been shown to be HPB in several reports, whereas R. planticola had not been reported as an HPB except in the case of strain ATCC 43176 (4, 10, 11). It is assumed that R. planticola had been misidentified as either K. pneumoniae or K. oxytoca due to a lack of R. planticola in the databases of commercialized systems. So we isolated nonmotile strains of HPB from fish with the agar used by Niven et al. (17) and identified them as either R. planticola or R. ornithinolytica by use of the identification system of Monnet and Freney (14). Moreover, we investigated nonmotile strains from stool specimens, provided strains, and reference strains for their histamine-producing ability. The purpose of our study was to clarify the identification of histamine-producing Raoultella strains and investigate the histamine-producing capability of Raoultella strains.

Top Abstract Introduction Materials and Methods Results Discussion References

 
Bacterial strains and identification system.
A total of 145 strains were examined. Twenty-seven nonmotile strains were isolated from fish, such as tuna, bonito, and sardines, with the agar used by Niven et al., which contains histidine and detects HPB (17). These strains showed the purple halo characteristic of a histamine-positive reaction on agar plates. Eighty-eight nonmotile strains were isolated from stool specimens with salmonella-shigella agar. The above-mentioned strains from fish and stool samples were identified with the following system. These strains were primarily identified with API 20E (Biomérieux). Then growth tests at 4 and 42°C (16, 18) and assimilation tests of four carbon substrates (14) were carried out for the final identification to the species level. The incubation times for the growth tests at 4 and 42°C were 7 and 14 days, respectively. The four carbon substrates were ethanolamine, histamine, D-melezitose, and DL-ß-hydroxybutyric acid (Sigma Chemical Co., St. Louis, Mo.). In addition to the above-mentioned strains isolated at the Osaka Prefectural Institute of Public Health, 17 provided strains were investigated (2 strains of R. planticola, 5 strains of R. ornithinolytica, 1 strain of Raoultella terrigena, 8 strains of K. pneumoniae, and 1 strain of K. oxytoca). We also examined the following 13 reference strains: R. planticola ATCC 43176 (American Type Culture Collection), IFO 3317 (Institute for Fermentation, Osaka, Japan), and IFO 14939; R. ornithinolytica ATCC 31898, JCM 7522 (Japan Collection of Microorganisms, Saitama, Japan), and JCM 7523; R. terrigena ATCC 33628 and IFO 14941; K. pneumoniae subsp. pneumoniae IFO 3512 and IFO 14940; K. oxytoca JCM 1665; K. pneumoniae subsp. ozaenae JCM 1663; and K. pneumoniae subsp. rhinoscleromatis JCM 1664. Morganella morganii JCM 1672 and Enterobacter aerogenes JCM 1235 were also employed as other HPB known to possess similar hdc genes (10, 23).

Histamine analysis of the Raoultella strains.
After cultivation overnight in Trypticase soy broth, aliquots (10 µl) of the bacterial cultures were transferred into 2 ml of Trypticase soy broth fortified with 1.0% histidine, pH 5.8 (TSBH) (22), and incubated at 30°C for 18 h. One-hundred-microliter aliquots were removed from each medium for measurement and diluted with distilled water (1:10 and 1:20 dilutions), and the histamine levels were measured with Histamarine (Immunotech, Marseille, France), an enzyme-linked immunosorbent assay kit, according to the manufacturer's protocol.

PCR amplification of the hdc genes.
The primers KPF2 (5'-AAA GCT GGG GGT ATG TGA CC-3') and KPR4 (5'-GTG ATG GAG TTT TTG TTG C-3') were designed on the basis of the hdc genes of R. planticola (GenBank and EMBL accession no. M62746). DNA amplification by PCR was performed in a reaction volume of 50 µl containing 0.75 U of Z-Taq DNA polymerase (Takara Biomedicals, Shiga, Japan), 25 pmol of each primer, and 5 µl of sample DNA purified by the benzyl alcohol-guanidine hydrochloride organic extraction method (7). Initial denaturation was carried out for 2 min at 94°C, and then 30 cycles of amplification were performed on a DNA thermal cycler (model 2400; PE Biochemicals Inc., Norwalk, Conn.). Each cycle consisted of three steps: denaturation for 5 s at 98°C, annealing for 5 s at 62°C, and extension for 5 s at 72°C. An additional step of extension for 5 min at 72°C was performed at the end of the amplification to complete the extension of the primers. Amplification products were detected by electrophoresis on a 1.5% agarose gel.

Preparation of the probe for the hdc genes.
A probe was prepared by PCR with genomic DNA of R. planticola ATCC 43176 as a template with the primers KPF5 (5'-TGC TAT CTG GGT CGG GAG AT-3') and KPR6 (5'-ATG CCC AGT TCG CTA ATT GA-3'). Labeling of the probe was achieved with a PCR digoxigenin probe synthesis kit (Roche Diagnostics Co., Mannheim, Germany).

Southern blot hybridization.
Genomic DNA was prepared with a DNeasy tissue kit (QIAGEN Inc., Chatsworth, Calif.), and 0.5 µg of the DNA was completely digested with restriction enzymes, electrophoresed on a 0.7% agarose gel, and vacuum transferred to a GeneScreen Plus membrane (NEN Life Science Products, Inc., Boston, Mass.). The membrane was prehybridized in ExpressHyb hybridization solution (Clontech Laboratories, Inc., Palo Alto, Calif.) at 50°C for 30 min, followed by hybridization at 50°C overnight with the same solution containing a probe labeled with 10-ng/ml digoxigenin. The hybridized probe on the membrane was detected by alkaline phosphatase-conjugated anti-digoxigenin antibody (Fab; Roche Diagnostics Co.). The enzyme-catalyzed color reaction was carried out with a nitroblue tetrazolium salt (NBT)-5-bromo-4-chloro-3-indolylphosphate (BCIP) system (Roche Diagnostics Co.).

Direct sequencing of the hdc PCR products.
The amplified DNA was directly sequenced with a BigDye terminator cycle sequencing FS Ready Reaction kit (PE Biochemicals Inc., Foster City, Calif.). The sequence of the labeled DNA sample was read by an ABI PRISM 310 genetic analyzer (PE Biochemicals Inc.) and analyzed with Factura software (PE Biochemicals Inc.).

Nucleotide sequence accession numbers.
The partial hdc sequence data for seven Raoultella strains reported in this study have been submitted to the DDBJ database and assigned accession no. AB075216 to AB075222 (inclusive).

Top Abstract Introduction Materials and Methods Results Discussion References

 
Identification of nonmotile strains from fish and stool specimens.
Twenty-seven strains from fish were identified as R. planticola (22 strains) and R. ornithinolytica (5 strains). Eighty-eight strains from stool samples were identified as R. planticola (21 strains), K. pneumoniae (51 strains), and K. oxytoca (16 strains). The identification results for a total of 145 strains are indicated in Table 1.

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TABLE 1. Number of positive reactions for the growth and assimilation tests of 145 strains

All the strains of R. planticola, most of which were able to grow at 4°C (46 of 48 strains) and utilize histamine (46 of 48 strains) and all of which utilized DL-ß-hydroxybutyric acid but not ethanolamine and D-melezitose (48 of 48 strains), were misidentified as K. pneumoniae or K. oxytoca by the API 20E system. A total of 48 strains of R. planticola and 13 strains of R. ornithinolytica are listed in Table 2. Thirty-six (17 strains from fish, 16 strains from stool specimens, and 3 provided and reference strains) of the 48 R. planticola strains showed a positive reaction to an indole production test.

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TABLE 2. Characteristics of the R. planticola and R. ornithinolytica strains studied

Histamine production by Raoultella strains.
All the strains from fish (22 strains of R. planticola and 5 strains of R. ornithinolytica) produced between 2,810 and 5,250 mg of histamine per liter in TSBH (Table 2).

In 88 strains of stool origin, 15 of 21 R. planticola strains produced between 2,610 and 5,200 mg of histamine per liter. The rest of the R. planticola strains (6 strains) and all the strains of K. pneumoniae (51 strains) and K. oxytoca (16 strains) produced no histamine.

With the 17 provided and 13 reference strains, 3 of 5 strains of R. planticola and all 8 strains of R. ornithinolytica also produced between 3,370 and 5,130 mg of histamine per liter. The rest of the R. planticola strains (2 strains) and all the strains of R. terrigena (3 strains), K. pneumoniae (10 strains), K. oxytoca (2 strains), K. pneumoniae subsp. ozaenae (1 strain), and K. pneumoniae subsp. rhinoscleromatis (1 strain) produced no histamine.

PCR detection of hdc genes.
Positive PCR results were obtained from all the histamine-producing strains (40 strains of R. planticola and 13 strains of R. ornithinolytica) (Fig. 1). Among the strains that produced no histamine (8 strains of R. planticola, 3 strains of R. terrigena, 61 strains of K. pneumoniae, 18 strains of K. oxytoca, 1 strain of K. pneumoniae subsp. ozaenae, and 1 strain of K. pneumoniae subsp. rhinoscleromatis), only 2 strains of indole-positive R. planticola (strains S8 and SJ10) showed positive PCR results. Regardless of histamine production, all 36 strains of indole-positive R. planticola showed positive results by PCR, as indicated in Fig. 1.

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FIG. 1. Amplification of DNA from Raoultella strains with the primers KPF2 and KPR4. Lane 1, molecular size markers (100-bp DNA ladder by New England BioLabs); lane 2, R. planticola ATCC 43176; lane 3, R. planticola IFO 3317; lane 4, R. planticola IFO 14939 (non-histamine-producing strain); lane 5, R. ornithinolytica ATCC 31898; lane 6, R. ornithinolytica JCM 7522; lane 7, R. ornithinolytica JCM 7523; lane 8, K. pneumoniae IFO 14940; lane 9, K. pneumoniae IFO 3512; lane 10, K. oxytoca JCM 1665; lane 11, R. terrigena ATCC 33628; lane 12, R. terrigena IFO 14941.

Southern blot hybridization.
Genomic DNAs of R. planticola ATCC 43176, R. ornithinolytica ATCC 31898, M. morganii JCM1672, and E. aerogenes JCM1235 were digested with three restriction enzymes (EcoRI, FspI, and PstI) and used as the reference strains in Southern hybridization experiments with the detection probe for the hdc genes. Hybridization signals were observed for four strains (Fig. 2). In both R. planticola and R. ornithinolytica, the probe hybridized to DNA fragments of 9.9 kbp when the DNAs were digested by EcoRI, 5.5 and 2.4 kbp when they were digested by FspI, and 1.8 kbp when they were digested by PstI. Since there is an FspI site within the probe-hybridizing area of R. planticola ATCC 43176, two fragments (5.5 and 2.4 kbp) were observed with this enzyme as expected. The patterns obtained from R. planticola ATCC 43176 and R. ornithinolytica ATCC 31898 were congruent.

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FIG. 2. Southern hybridization of HPB strains with the detection probe for the hdc genes. Genomic DNA was digested with restriction enzymes (EcoRI, FspI, and PstI). Lanes 1 to 3, R. planticola ATCC 43176; lanes 4 to 6, R. ornithinolytica ATCC 31898; lanes 7 to 9, M. morganii JCM 1672; lanes 10 to 12, E. aerogenes JCM 1235.

The genomic DNAs of 92 non-histamine-producing strains were digested with PstI for detection of the hdc genes. The hdc probe hybridized to 1.8-kbp DNA fragments of only two strains of R. planticola, S8 and SJ10. The lengths of the hybridized fragments in these two strains were equivalent to those of the fragments in the reference strains of R. planticola and R. ornithinolytica digested with the same restriction enzyme, PstI. The results of the PCR tests corresponded well with those of the hybridization.

Direct sequencing of PCR products.
PCR products from six strains of R. planticola (19-3, 27-1, 28-1, 42-1, Y1-1, and S8) and one strain of R. ornithinolytica (19-2) were sequenced and compared with the sequence of R. planticola ATCC 43176 (GenBank and EMBL accession no. M62746). The partial nucleotide sequence (685 bp) of the PCR products from the seven strains showed 97.2 to 99.4% identity to R. planticola ATCC 43176. Furthermore, R. planticola strain S8 and R. ornithinolytica strain 19-2 showed 100% identity.

Top Abstract Introduction Materials and Methods Results Discussion References

 
The histamine-producing strains were identified as R. planticola (40 strains) and R. ornithinolytica (13 strains), whereas a total of 61 strains of K. pneumoniae and 18 strains of K. oxytoca produced no histamine in TSBH and gave negative results for PCR and DNA hybridization of the hdc genes. A group of histamine-producing strains were classified as K. pneumoniae when Taylor et al. and Niven et al. reported HPB in fish in 1979 and 1981, respectively (17, 20). Afterward, this group's identification was changed from K. pneumoniae and K. oxytoca to K. planticola and K. ornithinolytica when K. planticola and K. ornithinolytica were distinguished from K. pneumoniae and K. oxytoca as new species. These two Klebsiella species have since been classified in the genus Raoultella.

K. pneumoniae and K. oxytoca have been considered to be the most important HPB isolated from fish even after K. planticola was described as a new species (12, 13). So far, R. planticola has not been reported as an HPB, except in the case of one strain, ATCC 43176 (8). Histamine-producing strains of R. planticola appear to have been misidentified as either K. pneumoniae or K. oxytoca by conventional methods used in the identification of HPB (11, 13). R. planticola cannot be distinguished from K. pneumoniae and K. oxytoca with the commercialized systems, because K. planticola (R. planticola) is not included in the databases of these systems (14). In fact, 48 collected strains of R. planticola were misidentified as K. pneumoniae or K. oxytoca by the API 20E system. R. ornithinolytica has also not been reported as an HPB, although commercialized systems are able to identify it. However, R. ornithinolytica was isolated as an HPB from fish and was found in the present study to be equivalent to R. planticola in its histamine-producing ability.

We demonstrated the importance and efficiency of Monnet and Freney's method for the identification of histamine-producing Raoultella strains (14). For the histamine assimilation test, R. planticola and R. ornithinolytica gave positive results but K. pneumoniae and K. oxytoca gave negative results. It is reasonable to postulate that histamine-utilizing species (R. planticola and R. ornithinolytica) are able to produce histamine and that non-histamine-utilizing species (K. pneumoniae and K. oxytoca) are unable to produce histamine. Another histamine-utilizing Raoultella species, R. terrigena, produced no histamine, although only three strains were investigated. R. terrigena was isolated mainly from nonclinical origins (soil and water) (9). It may be that R. terrigena contaminates fish; however, R. terrigena strains were not isolated as HPB from fish in the present study.

R. planticola and R. ornithinolytica are able to grow slowly at 4°C. Moreover, these strains are often isolated from raw fish and fish products. The low-temperature growth response and environmental distribution of histamine-producing Raoultella strains are notable with regard to food hygiene. There was no difference in the histamine-producing capabilities among the histamine-producing strains regardless of their sources. All the histamine-producing Raoultella strains produced a large amount of histamine. There is little doubt that R. planticola and R. ornithinolytica are the most important HPB that cause HFP.

 
We thank K. Tamura (National Institute of Infectious Diseases, Tokyo, Japan) for providing the R. planticola, R. ornithinolytica, and R. terrigena strains and M. Yasuoka (Tsukuba University, Ibaraki, Japan) for providing the K. pneumoniae and K. oxytoca strains. Our thanks also go to H. Shibata, K. Mizukoshi, and S. Hirata, Osaka Prefectural Health Center, for their devoted support for this study.

 
* Corresponding author. Mailing address: Osaka Prefectural Institute of Public Health, Nakamichi 1-3-69, Higashinari-ku, Osaka 537-0025, Japan. Phone: 81-6-6972-1321. Fax: 81-6-6972-1329. E-mail: kanki{at}iph.pref.osaka.jp.

Top Abstract Introduction Materials and Methods Results Discussion References

 

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Applied and Environmental Microbiology, July 2002, p. 3462-3466, Vol. 68, No. 7
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.7.3462-3466.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

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