Evaluation of histidine decarboxylase activity of bacteria isolated from sardine (Sardina pilchardus) by an enzymic method

Letters in Applied Microbiology 1994, 19, 70-75

Evaluation of histidine decarboxylase activity of bacteria isolated from sardine (Sardina pilchardus) by an enzymic method

E.I. Lopez-Sabater, J.J. Rodriguez-Jerez, M. Hernandez-Herrero and M.T. Mora-Ventura Department of Food Hygiene, Faculty of Veterinary Medicine, Universidad Autonoma d e Barcelona ( U A 8 ) ,

Barcelona, Spam

GWG 230 accepted 7 February 1994

E I . L O P E Z - S A E A T E R , J . J . R O D R I G U E Z - J E R E Z , M . H E R N A N D E Z - H E R R E R O AND M T.

M O R A - V E N T U R A . 1994. A t i s t and simple enzymic method has been adapted t o measure histidine decarboxylase activity in bacteria isolated from tish. I t was possible t o quant i fy t h e presence of his taminc at Ievels higher t h a n 1.03 x 10 - 2 p m o l ( 3 ppni ) per ml of cul ture m e d i u m . 'I'here was a good correlation ( v = 0.99) between t h e his tamine content a n d t h e increase of absorbance i n t h e concentrat ion range of 3 a n d 30 p p m . 'I'he method can b e used for quant i ta t ion of t h e a m o u n t of histamine produced by a selected s t ra in , a n d has t h e advantages of being low in cost, reliable, easy t o use a n d f i s t t o per form. P l t w ~ m o n ~ t s shrgelloirles, a bacter ium frequent ly isolated from tish a n d aquat ic environments , has been identified as ;I new histamine-former in fish.

INTRODUCTION

I he term biogenic aniines is used to signify those non- volatile amines such as histarnine, cadaverine, putrcscine, sperminc, spermiclinc, tyramine and tryptaniinc, which ;ire formed by decarhoxylation from their respective precursor amino acids. T h e presence of high concentrations of these amines, particularly o f histamine, is the result of microbial activity, espccially that of mesophilie bacteria, rather than the consequence of autolysis. klistaniine has a great signifi- c ~ n c e in fish both as a spoilage indicator and as a public h d t h hazard. Thus, thc J:lX: has recently established regulations tor species of fish belonging to the Scombridae and Clupcidae families and tixcd 100 ppni of histamine as thc limit of acceptance (Anon. 1991).

A number of workers have studied the histidine deoar- hoxylase activity of bacteria isolated from fish and several culture broths have been proposed to assess the enzymic activity. In order to evaluate ;i rnicro-oraanisni's ability to produce histamine in tunafish Ornura L'/ [ I / . (1078) developed a medium from an extract of fresh skipjack tuna ( Ihihynnus prlurnis) ( 'WID). This method was later niodi- fied by Arnold r / ' r l . (l9XO), Yoshinaga and Frank (10x2) and Iiamesh e/ 111. (1080). Ababouch ' I / . ( I O O I ) further

r 7

modified the coniposition of the medium using sardine (SI?lH) insteiid of skipjack. Nevertheless, the aforementioned broth has some drawba , I t is difficult to prepare, as its final composition can vary enormously depending on the spccics and the quality of the fish used as raw material (Taylor and Woychili 10x2; Yoshinaga and Frank 19x2).

These flilings were overcome hy 'I'aylor el a / . (107X) who developed a simple method to quantify the formation of histamine by micro-organisms of the I-nterobacteriaceac t:aniilg. 'I'hc culture medium consisted of a trypticase so!

broth supplemented with 0.1 ''4) histidine niono- hydrochloride ('I'SHH) with the p H adjusted to 6.8 . However, 'I'aylor and Woychih (1082) observed that neither the histicline content nor the p H o t the culture medium were the most appropriate to ensure maximum histamine famiation. 'I'hus, they increased the histidine content to 2% and adjusted the pH to 6 . 3 . 1:ranh t ~ / id. (10X.5) further moditietl the composition hy adding 0.01 'h pyridoual hydrochloride :is a co-tictor.

Initially, bacterial histidine ttcc;lrbox).l;ise activit! was measured by means of a Warhurg manometer, wing the ( X I 2 volume released i n the culture broth. I lowever, thi.; method has fiCillcn into disuse. Nowadays, the histamine produced in the culture broth is measured chieflj by means of high-pressure liquid chromatograph! (HPIX:), spectro- fluorimetr) and thin layer chromatograph! ( T I .C). All the aforementioned techniques, with the exception of '1'1 ,[;-

H I S T I D I N E D E C A R B O X Y L A S E I N B A C T E R I A 71

require costly and sophisticated equipment, specially trained staff and lengthy preparation of the extract of the sample to be analysed.

Sumner and Taylor (1989) developed a method for detecting histamine-producing lactic bacteria, using leucocrystal violet ( I L V ) and diamine oxidase (1lAO). This qualitative technique made it possible to detect bacteria capable of producing more than 1.2 pmol of histamine per nil. However, i t was unsuitable as a quantitative technique due to interference from the culture broth (Sumner and Taylor 1989). A modification of this method has proved to be a simple, speedy and low cost technique for determining histamine content in fish (1,bpez-Sabater rt ( I / . 1903). 'The authors' aim was to adapt a Fast and simple enzymic method on the basis of work previously carried out hy I,crke ct u / . (1983) and Sumner and Taylor (1980), which would enable the quantification of histidine dccarhoxylase activity in bacteria isolated from fish and, in general, an! foodstuff likely to have a high histamine concentration. In addition, the identification of bacteria responsible for histamine production in sardine and their capacity to form histamine were also studied in the present work.

MATERIALS AND METHODS

Bacterial strains

Sardine (Sordina pilchardus) caught in the Mediterranean Sea wcrc iced in boxes and transported to the laboratory where the! were stored in air-permeable plastic bags at two different temperatures (8" and 20°C) until the fish were spoiled. A t different intervals depending upon the tcni- perature used (12 h and 4 h respecticcly), 10-g samples of tish flesh were removed aseptically and homogenized for 5 niin with sterile 0.1'%, peptone water (Ilifco) in ;I Stoni- acher 1,ah-Blender 400. '1'0 isolate histamine forming bacteria, appropriate serial decimal dilutions were prepared in 0.1 '% peptone water. Duplicate plates of Niven's medium modified by Smith el al. (1082) (autoclavcd at 121°C for 7 min) were inoculated, covered with an overla! of the same medium, and incubated in aerobic conditions a t 37 C: fix 48 h. Forty strains that changed the pH indicator in Niven's medium were selected. T h e isolates are listed in 'I'able 1. 'I'he bacteria were stored refrigerated until use on trypticasc soy agar ( T S A ) (Difco) slants supplemented with 0.1 '%, 1.-histidine-H(:l (Aldrich Chemical) and the pH w a s adjusted to 6.0.

Decarboxylase activity

'1'0 avoid the interference caused by reducing sugars in the culture media, a broth (NN) containing the following coni-

position (g I ~ '1 in distilled water was developed : tryptonc, 5 ; NaCl, 5 ; K211P0 , , 2.5 ; and r.-histidinc-II(:l, 10. Final p I I was adjusted to 5.3.

A loopful obtained from a pure culture grown for 24 h in trypticase soy agar (Ilifco) supplcmcnted with 0.1"4, histidine-HCl was inoculated on 0 ml of V13 broth. Cul- tures were incubated without shaking at 37°C for 24 h. Then, 1 nil was further transferred t o another tube containing 0 ml of NR hroth and incubated at 3 7 ' C for 18 h (Sumner and 'I'aylor 1989). 'I'his inoculum was approx- imately equivalent to Io' cfu mI I .

Five millilitres of this broth culture were taken with a sterile syringe and sterilized by filtration through a 0.22-pm membrane (Millipore). 1:iltrates were stored at - 26 C until assayed. 'I'hc filtration ohjectivcs were to stop hista- niinc formation and to avoid the turbidity caused by cells that could interfere with the opticill density readings. 'I'otal plate count was dctcrmined in the remaining unfiltered broth. Of appropriate decimal dilutions prepared in 0.1 "4 peptonc water, duplicate 1 nil volumes \!ere plated on trypticase soy agar ('I'SA) (Difco) containing 0 - 1 '%I I.-

histidine-HCl and incubated at 37 (; for 48 h.

Reagents

Solutions of 1)AO (Sigma Chemical Co.) and H K P (Sigma (:hemica1 Co.) were prepared according to IApez-Sabater r / NI. (1993) in twice-distilled water with 0.35 UI ml ' and 17.24 U I ml I respectively. T h e enzyme solutions were prepared daily. 'I'hc leuco crystal violet (1-CV) (Aldrich (:hemica1 Co.) in O..5Yl HCI and the phosphate hutfcred solution (0 .1 .5 niol 1 I , p I I 6.8, a mixture ofKIH,PO, and Na,HPO,) were prepared according t o 1,erke et d. (1983). Oncc prepared all reagents were stored between 0 and 2 C. T h e I . C V solution was also Lept protected from light. All reagents used were of. analytical grade.

I he standard solutions were prcparcd directly in N13 broth, trypticasc soy broth and phosphate buffer M ith histamine dihydrochloridc (hlerck). Concentrations bctwecn 3 and 30 ppni of histamine as free base were used.

, >

Histamine analysis

'I'hc filtrates from the broth cultures Mere thawed at room temperature and malyscd for histamine by means of an enzymic method. T h e method was h a d on the action, a t a p H of 6.8, of diainine osidase enzyme ( 0 . j ml) on the histamine present both in the broth or in the standard to be analysed ( 0 . 5 nil). As products of enzymic activity, imid- azole acetaldehyde, ammonia and hydrogen peroxide were ti)mied. A second enzyme (pcrosidasc) (0.5 ml), in the

72 E. I . L O P E Z - S A B A T E R E T A L .

Table 1 I Iistiiline tlccarhoxylase activit) of strains isolated from sardine tested in Activity 1 Strain Organism I listanline* Count t

N-3 1 N-4 N-18 N-24 N-39 N-29 N-50 N-28 N-30 N-I9 N-20 N-42 N-33 N-37 N- 1 h N-38 N-22 N-1.3 N-I4 N-40 N-48 N -27 N-23 N-44 N-4.5 5-9 N-2 1 N-32 N-3 N- 1 N-2 N-36 N-25 N-12 N-1.5 N-47 N-8 N-17 v-34 N-41

icgglonirru ns

Plesromonas .shi~eNoiJes

NIJ broth b y micans of the enzyniatic .5. I002 .5 ,317 .i method proposcd

8.4527 10.7 120 10.0170 0 4 . 3 7 2 , 2 0 2 6 0.01 2 0 0.0208 0.01 88 04743 0~0000 0.1 120 0.1 I00 0 4 2 2 1 O.IOl7 04~240 0.1 533 0.1383 0.042X 0 ~ 0 3 x 1 0.0373 0.0455 04372 0.0381 0~0000 0 4 2 0 0 0.2630 0.0450 0.06 13 0 4 3 5 2 04373 040 1‘) 0 . 0 5 I 2 0.01 87 04704 1.0296 0.1007 0.0406 0.1260

* hleasured as ppm. t hlcasured as log cfu g ~ I.

3 hlcasured as pmol ml ~ I 18 h $ Nl) denotes ‘none dctected’ or < 3 . 0 ppni, the minimum level of reliable measurements.

I a t 37 (:,

presence of a chromogen (1,CV) (0.1 nil) in reduced form (colourless), caused its oxidation into crystal violet (coloured form). After incubation a t 37°C: tor 2 h, the Under the conditions described, a linear relationship appearance OF colour was measured with a 13ausch & 1.ornb between optical density and histamine concentration in Spectronic 201 1 at S O 6 nm. the NB broth was observed over the range 3 to 30 ppni ot‘

R E s U LTS A N D D I S C U s s 10 N

Corrigendum

Biodegradation of phenanthrene by Phanerochaeie chrysosporium: on the role of lignin peroxidase

M. Tatarko and J. A. Bumpus

Letters in .4pplird Microbiology 1993, 17, 2&24

Figure 5 (the proposed pathway for phenanthrene oxidation by Phanerocaete chrysosporiurn) should be represented as follows :

H

I m. TL

J

Corrigendum

The effect of incubation temperature, sodium chloride and ascorbic acid on the growth kinetics of Aeromonas hydrophira

Mara Lucia Stecchini, lleana Sarais and S. Milani

/,ettrrs in Applied M t t r o h i u l o ~ y 1093, 17, 238-241

Thc ascorbic acid concentration$ in the text and the tables should bc 1 mmol I ' and 2 mmol I ~ I instead of 0.1 mmol I and 0.2 mmol I '.

Erratum

CCD-monitoring of bioluminescence during the induction of the cell wall-deficient, L-form state of a genetically modified strain of Pseudomonas syringae pv. phaseolicola

Rosemary N. Waterhouse and L. Anne Glover

l ,c / ter \ i n .4pplwJ M i r vohioloqy 1004, 19, HX 01

r . 1 he printers, Cambridge University Press, regret the incorrect running order of this paper published in Letters in : Ippl te~l Mirrohiokogy Volume 10, Numhcr 2 ( 1994).


1.0-

0 . 8

0.6- 0 n ::

1 0 4 -

0 2 -

histamine per ml of culture medium ( r = 0.9045, P < 04OI). T h e coefficient of variation (CV) was 2.9'%,. 'The present investigation has confirmed, as indicated by Sumner and 'Taylor (1989), that the 30 min recommended by I.erke ( 'I al. (1983) does not allow for adequate coloration in the reaction. By increasing the incubation period to 2 h, results arc considerably improved and a clear differen- tiation bctween positive and negative results is possible.

T h e limitations indicated by Sumner and Taylor (1989) in the use of this method to quantify histidine decarhoxylase activity have been rectified. By filtering the culture medium, the turbidity caused by the growth of bacteria was removed. Similarly, by using a colourless broth (NB) the interference caused by the coloration of the culture medium referred to by Sumner and Taylor (1989) was avoided. All these observations indicate that the method described can be used for quantitation of the amount of histamine produced b) a selected strain or a mixed culture. This method measures lower histamine levels (041 pniol ml I ) than were obtained by Sumner and Taylor (1989) (1.2 p o l ml I ) . I t has the advantages of being low in cost, reliable, easy to use and fast to operate.

Substantial improvements were achieved using the culture broth developed in this study, as compared with a 'TSBH broth (Fig. I ) . There is a clear parallelism between the regression lines obtained with 'I'SRH and the NB broth. I lowever, whilst the regression line obtained with the NIj broth did not differ significantly ( P = 0.5765) from the best results observed in the regression line using phosphate buffer as solvent, the difcrences found in T S B H were highly significant ( P < 04Ol). Probably, this was due to the high content of reducing sugar present in the com- mercial TSR broth. Pavelka (1982) and Huang et al. (1988)

-

I I 0 5 10 15 20 25 30

Histamine ippm)

Fig. 1 Kegression lines tor histamine ?'.r optical density from stmdard solutions prepared in TSBH (e), NR broth (m), and phosph;itc h u t k r (A)

have pointed out that as a result on non-enzymatic browning reactions, dextrose may react with the histamine and histidine present in food, thus giving rise to the formation of Amadori compounds. For the concentrations of histamine used, the values of absorbance obtained by using the ' I 3 R H broth were excessively low, between 0 and 0 . 3 units, giving a very low density colour. 'I'hercfore, in some instances bacteria isolates unable to produce histamine can be erroneously identified as weak histamine-formers (filse histamine-formers) in 'I'SBH broth. In contrast, however, the N13 broth allowed clear separation, even between weak histamine-formers and non-histamine producing bacteria.

All isolates were Gram-negative. O f the 40 strains isolated from Niven medium that were able to produce a spe- cific change in the indicator (broniocrcsol purple), 77..5'% belonged to the Ilnterobacteriaceae family, 20'% to the Vib- rionaccae Gamily (Pkrsronzonas genus), and 2..5'!+, to the Pseudonionadaceac family. 'The single most frequently encountered species was Enterohactrr qglonrerans ( 1 1 isolates). Most of the bacteria isolated in this study have already been reported as histamine-formers from fish, meat and dairy products. I Iowever, Pliwomonrrs shigelloidcs (8 isolates), Cedererr Iupagri (1) and Cedeuri neteri ( I ) have not previously been considered in the literature to be responsible for histamine formation in fish. They were all identified as weak histamine-formers ( < 30 ppni) and, therefore, of little health-related significance.

Of isolates identified, all except Pkr. shigrllozdrs d o not appear as part of the natural microflora of newly caught sardine. Probably, many of them might be expected to be found as a result of human contamination of the fish during capture and improper handling. Yamani and L' jntermann ( 1985) have pointed out that histamine-forming bacteria are ubiquitous organisms, particularly in food handling estab- lishments and, therefore contamination is virtually unavoid- able after fish have been captured. In contrast, Plr. s h z ~ r / l o i r / r s has frequently been isol;tted from fish and aquatic environments, and some worhcrs have implicated it was the causative agent of several epidemic outbreaks of diarrhoea associated with eating uncooked shellfish or fish (1,iston 1990). I t accounted for 20'% of the total histamine-producing isolates. T h e histamine content produced by Pie. shi~rlloidrs after 18 h at 37' C: ranged between 3 . 5 ppni and 48.5 ppm. In spite of having optimum growth bctween 37 and 38 C:? I'kr. shigrlknrdrs is able to grow at 8' C. This observation suggests that PIr. shzgrllordrs could be responsible for the histamine fornicd when fish is stored at low temperatures. Fiowever, the rate of production of histamine by Plr. shigrlkordrs, even when incubated at its optimum temperature, is too slow to represent a serious hazard for consumers.

All the strains showed similar growth in the NR broth. ' I ' herche , the differences in the amount of histamine pro-

74 E I L O P E Z - S A B A T E R ET AL

duced are attrihutable solely to dilferences in the activity of their respective enzymes. T h e amounts of histarnine formed in the NB broth are presented in 'I'able I . Isolates that produce more than 0.01 pmol of histamine per ml of culture broth showed a positive reaction. Thirty-eight of 40 isolates produced detectahle amounts of histamine in the culture broth after 18 h at 37'<:, as measured by the enzymic method. I Iowever, of the 38 positive isolates only i+forguni41u rnorgunri and /.'scurlornonus arrirginosrr produced significant amounts of histamine. In some instances, the hisramine amount elaborated by P r . nwrxuriii strains corre- sponded to an almost total conversion of' the free histidine present in the N13 broth. O n l y two trl' isolates from Niven medium, En&. clour.ar N-42 and Ln/. ugg/om(wns N-9, did not show histidine dccarhoxylasc activity in the culture medium.

Ikhling and 'I'aylor (1082) divided histidine decarboxyl- asc bacteria into two groups: ( I ) bacteria capable of producing more than 1000 ppm of histamine in a culture medium after 24 h of incuhation at 15 'C; and (2) bacteria incapable of producing 250 ppm of 1iist;imine in a culture medium after 48 h of incubation at 3 0 (:. If the above mcn- tioned classification is applied to the results of this study, only 3 (all Mar. rnorguncr) of the 40 strains could be considered to have a high enzymic activity and would be capable of producing toxic concentrations of histamine in a short period of' time in fish when i t is not stored in iidc- quatc refrigeration conditions. 'I'hc maximum histamine concentration produced by a single .&for. morgunii isolate in this study was 2009.5 ppm. This amount was 20 times higher than the limit of acceptancc established by the 13TC (I00 ppm) for histamine content in fish. The present results are in accordance with those reported b y Catraneo et al. (1984), who observed on mackerel and tunatish caught in the Mediterranean Sea that only Mor. morgunir was able to produce large quantities of histamine. As many authors have pointed out M o r . rnnrganrr is also the main histamine- producer in fish from the Mediterranean Sea and a fiirly coninion contaminant in these kinds of food products. 'I'hus, even though nobody has yet proved that histamine per SP is the causative agent of scomhroid food poisoning, the authors consider that .&for. n2argcrnir should be moni- tored in fishery products after harvest and through handling the processing to control the histamine formation.

ACKNOWLEDGEMENTS

'I'hc authors gratefully acknowledge support of this work hy the Coniisii)n 1 ntcrministcrial de (liencia y 'I'ecnologia ((:I( :\''I.), Ministeritr de Educacibn y Ciencia, Spain (Project AI~IXO-OO~O-C0.?-02).

'I'he authors wish to thank k1.C:. I-lerrador-Kius and A.X. Roig-Saguks for providing assistance in the laboratory

work. T h e co-operation of' our colleague hlr X. Ihsch- Sagrera is also gratefully acknowledged. In addition, we thank I h 1 . (:amOn-Urgel for critically reading the manu- script.

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Documents

Evaluation of histidine decarboxylase activity of bacteria isolated from sardine (Sardina pilchardus) by an enzymic method