Beta-Indoleethanol and Beta-Indolelactic Acid Production by
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1 ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, Mr. 1976, p Copyright C 1976 Americn Society for Microbiology Vol. 9, No. 3 Printed in U-SA. Bet-Indoleethnol nd Bet-Indolelctic Acid Production by Cndid Species: Their Antibcteril nd Autontibiotic Action T. K. NARAYANAN AND G. RAMANANDA RAO* Microbiology nd Cell Biology Lbortory, Indin Institute of Science; Bnglore , Indi Received for publiction 19 September 1975 Cndid spp. grown in synthetic medium supplemented with L-tryptophn s sole nitrogen source produced /B-indoleethnol (/3-IEA) nd /3-indolelctic cid (/3-ILA). These compounds isolted from the culture filtrtes were chrcterized by ultrviolet, infrred, nd nucler mgnetic resonnce spectrl studies. Using DL-[3Hltrypotophn in the medium, lbeled (3-IEA nd /3-ILA were isolted. Further, /3-IEA ws produced s result incubting log-phse cells of C. lbicns with /3-ILA. Both (3-IEA nd A3-ILA inhibited the growth of grmpositive nd -negtive bcteri. Autontibiotic ction of these compounds on Cndid spp. nd the reversl of this inhibition were studied. Cndid spp. produced f3-phenethyllcohol (5, 7) nd its corresponding hydroxy cid, (- phenyllctic cid (7). The utontibiotic ction of (-phenethyllcohol hs lso been reported (5, 6). Production of /8-indoleethnol (tryptophol;,8-iea) nd,b-indolelctic cid (/3-ILA) byagrobcterium tumefciens (3), Diplodi ntlensis (1), Acetobcter xylinum (4), Aspergillus niger (2), nd Rhizobium spp. (8, 9) hs been described. In this pper we report the production nd quntittion of,b-iea nd /3-ILA by both pthogenic nd nonpthogenic species of Cndid grown in the presence of L-tryptophn s the sole source of nitrogen. These compounds hve lso been exmined for their ntibcteril nd utontibiotic ction. MATERIALS AND METH ODS Orgnisms. Cndid lbicns Z248, C. guilliermondii Z55, C. krusei Z70, nd C. tropiclis Z56 were obtined from the London School of Hygiene nd Tropicl Medicine, London, nd C. intermedi ws obtined from the V. P. Chest Institute, New Delhi, Indi. Stock cultures were mintined on Sbourud glucose gr. Escherichi coli, Proteus vulgris, Prcolobctrum erogenoides, Aerobcter erogenes, Bcillus subtilis, B. megterium, nd B. cereus were from the culture collection of this lbortory nd were mintined on nutrient gr slnts. Isoltion of compounds. The growth of orgnisms nd the procedure for the isoltion ofcompounds nd their purifiction were similr to those described erlier (7). Spectr. The infrred spectr were tken in Nujol in Crl Zeiss model W10 spectrophotometer nd the nucler mgnetic resonnce spectr of the compounds (10 to 15%) were tken in Vrin model T60MHz. The ultrviolet spectr of the compounds 375 in queous solution (10 mg/100 ml) were obtined in Unicm SP 700A recording spectrophotometer. Reversibility of growth inhibition cused by 13 IEA nd,&ila. Side-rm Erlenmeyer flsks (250 ml), ech contining 100 ml of medium (described in Tble 5), were inoculted with 1 ml of 24-h broth culture in the sme medium. After 8 h of incubtion on rotry shker (200 rpm) t 30 C, the compounds were dded septiclly to two flsks nd incubted further for nother 8 h. The cells thus exposed to the compounds were centrifuged nd wshed four times with sterile medium, suspended in the sme volume of fresh medium, nd incubted. The culture filtrte from the flsk to which j3-ila ws dded ws extrcted using the isoltion procedure previously described, nd the product ws identified by chromtogrphy. RESULTS AND DISCUSSI ON The physicochemicl properties of,b-iea nd,8-ila re shown in Tble 1. The infrred spectrum of p-iea is shown in Fig. 1. The ssignments of the peks re s follows: (i) shrp pek t 3,400 cm-' corresponds to N of indole nucleus; (ii) brod H pek t 3,200 cm-' corresponds to C1-OH, which is mostly hydrogen bonded; (iii) peks t 1,430, 1,470, nd 1,620 cm-' show tht it is n romtic compound; (iv) peks t 1,050, 1,100, nd 1,190 cm-' further support the presence of the -OH group. The infrred spectrum of f8-ila is shown in Fig. 2. The ssignments of the vrious peks re s follows: (i) shrp pek t 3,400 cm-1 corresponds to N ; (ii) pek t 3,500 cm-' H
2 376 NARAYANAN AND RAO TABLE 1. Physicochemicl properties of (3IEA nd,b-ila isolted from culture filtrte of Cndid species Property (3-IEA,B-ILA Liquid/solid Crystlline leflet Microcrystlline powder Odor Fecl odor Fecl ordor Melting point (C) Solubility in: Acetone Highly soluble Highly soluble Chloroform Soluble Springly soluble Ether Soluble Soluble Wter Springly soluble Soluble Ultrviolet spec trum (X.") (nm) Opticl rottion +6 t 30 C (c. 2.5 in ethnol) R, vlue b Thin-lyer chromtogrphy solvent system: petroleum ether (40 to 60 C)-ether (15:25, vol/vol); identifiction by iodintion. b Pper chromtogrphy solvent system: benzene-cetic cid-wter (15:6:3, vol/vol/vol); identifiction by sprying with 0.1% KMnO4. corresponds to C2-OH; (iii) shrp peks t 1,700 nd 1,720 cm-' correspond to 0=0; (iv) peks t 1,400, 1,480, nd 1,640 cm-' show the romtic nture of the compound; (v) peks t 1,080, 1,100, nd 1,200 cm-' further support the presence of the -OH group. The nucler mgnetic resonnce spectr of f8- IEA re shown in Fig. 3 nd 4. A multiplet centered t 7.48 corresponds to the indole nucleus. The triplets t 3.98 (J 6Hz) nd 2.98 (J ANTIMICROB. AGENTS CHEMOTHER. 6Hz) correspond to two -CH2-groups coupled to ech other. A shrp singlet t 28 nd brod singlet t 8.28 correspond to Cl-OH nd N H of indole, respectively, which dispper on D2O exchnge (Fig. 3). The shift of the singlet of C,-OH in Fig. 3A is due to the concentrtion difference. A singlet t 4.78 in Fig. 4B is due to HDO. The bsence of methyl group singlet between 18 nd 28 nd the presence of two triplets indicte tht the indole nucleus is seprted from C1-OH by n ethylene linkge. The nucler mgnetic resonnce spectrum of /3-ILA shows multiplet signl similr to (3- IEA centered t 7.48, corresponding to n indole nucleus (Fig. 5). The two qurtet signls t 4.28 (J 5Hz) nd 3.28 (J 5Hz) indicte tht pro- H H tons of - nd -C- re coupled to ech H other. The signl t 2.58 is due to Me2SO. The physicochemicl nd spectrl properties of the isolted compounds re identicl to uthentic,b-iea nd A3-ILA (Sigm Chemicl Co., St. Louis, Mo.). All Cndid spp. tested produced both (8-IEA nd (3-ILA (Tble 2). C. guilliermondii nd C. krusei produced more (3-IEA nd less A-ILA. The reverse is the cse with the other three species. This pttern of producing either lcohol or hydroxy cid in excess is similr to the production of (3-phenethyllcohol nd its corresponding hydroxy cid, (3-phenyllctic cid (7). The totl yield of 3-IEA nd /8-ILA rnged from 14 to 24% mong Cndid spp., s FIG. 1. Infrred spectr of isolted nd uthentic (3IEA (tryptophol).
3 VOL. 9, 1976 PRODUCTION OF f3-iea AND,-ILA BY CANDIDA SPP. 377 WAVE NUMIR (c m'1) FIG. 2. Infrred spectr of isolted nd uthentic,-ila. S S PPW () FIG. 3. Nucler mgnetic resonnce spectr of (A) isolted nd (B) uthentic /9IEA.
4 AVn"9mlc IW.3/A 46 JlJ A* AD -H (A)l o 7.0 so so PPM (6X FIG. 4. Nucler mgnetic resonnce spectr of(a) isolted nd (B) uthentic f-iea fter D20 exchnge PPM (61 FIG. 5. Nucler mgnetic resonnce spectr of (A) isolted nd (B) uthentic 3-ILA. 378
5 VOL. 9, 1976 compred to 34 to 67% of 83-phenethyllcohol nd,3-phenyllctic cid together (7). Lbeled f3-iea nd /8-ILA hve been isolted by using DL-[3H]tryptophn (5T) (Tble 3). Approximtely 17% of the tryptophn tken up by the cells is found converted to /3-IEA (specific ctivity, 0.21 IACi/mmol) nd /3-ILA (specific ctivity, 0.165,uCi/mmol). The specific ctivities of both lbeled compounds remined the sme fter repeted purifiction.,83-ea inhibited the growth of both grmpositive nd -negtive orgnisms in the concentrtion rnge of 6 to 12 mm (Tble 4). However, grm-negtive orgnisms in generl re more susceptible thn grm-positive orgnisms. Like TABLE 2. Yests Production of f3iea nd 3-ILA by Cndid species Yield (mg/liter of medium contining 1 g of L-trypotophn) PRODUCTION OF,B-IEA AND /8-ILA BY CANDIDA SPP. 379 % Con- version,8-iea /3-ILA of L- tryptophn dded C. guilliermondii C. krusei C. intermedi C. lbicns C. tropiclis The medium used consisted of: glucose, 20 g; KH 2PO4, 3.5 g; MgSO 4-7H 20,2.5 g; CCl 2-2H 20,2.5 g; L-tryptophn, 1 g; nd biotin, 30,ug; distilled wter to 1 liter. Cells were grown t 31 C for 2 dys on rotry shker. TABLE 3. Isoltion of [3-3H]IEA nd [3-3H]ILA from culture filtrtes of C. intermedi Tryptophn Counts/ min Amt dded.3 X 106 Remining fter the extrction of culture filtrte x 106 Tken up by the cells x 106 Converted to: /3-IEA (28.2 mg) x x 10,8-ILA (122.8 mg) x 10O5 Cells were grown in the medium described in Tble 2, which ws supplemented with 10,uCi of DL- [3H]tryptophn (5T) (1,600 mci/mmol) obtined from BARC, Bomby, Indi. The compounds were isolted s described in the text, nd rdioctivity ws mesured in Beckmn LS-100 liquid scintilltion counter. About 17% of the tryptophn tken up by the cells ws found to be converted to (-IEA (4.6%) nd /8-ILA (12.4%).,83-EA, /8-ILA lso inhibited the growth of E. coli t 6 mm nd B. cereus t 15 mm. The utontibiotic property of,3-iea on Cndid spp. is reveled by the dt in Tble 5. All species exmined were totlly inhibited t concentrtions of 6 to 12 mm. However, C. tropiclis, which produces the lowest level of 3l84EA, is highly susceptible to /3-lEA s compred with other species. This ws lso observed with /3- phenethyllcohol (6). Some dt illustrting the nture of inhibition exerted by,b-ea nd /8-ILA on the growth of C. lbicns re shown in Fig. 6. When,3-IEA ws dded to log-phse cells, no further growth took plce. The inhibition of growth ws seen s long s the cells were in contct with p8-ea. After wshing the cells free of /8-lEA, the cells exhibited growth pttern similr to the control. This clerly shows the reversible nture of the inhibition by 8-TEA. A similr effect is exhibited by,b-ila s well. The inhibition TABLE 4. Influence of /3IEA on the growth ofgrmpositive nd grm-negtive bcteri % Inhibition Orgnism mm 6mM 9mM M mm mm Escherichi coli Prcolobctrum ero genoides Proteus vulgris Aerobcter erogenes Bcillus subtilisb Bcillus cereusb Bcillus megteriumb TEA concentrtion. bsince Bcillus spp. form pellicles, the growth inhibition is grded visully. Nutrient broth (5 ml) ws inoculted with 0.1 ml of n 18-h culture nd incubted t 37 C for 24 h. Growth ws mesured in Klett-Summerson colorimeter t 540 nm. TABLE 5. Autontibiotic effect of /3-IEA on growth of Cndid species % Inhibition Species 3 MM 6 mm 12 mm 18 mm C. lbicns C. tropiclis C. krusei C. guilliermondii C. intermedi ,8-1EA concentrtion. b The medium used consisted of glucose, 20 g; KH 2PO4, 3.5 g; (NH 1) 2SO4, 2.5 g; MgSO 4,7H 20, 2.5 g; CCl2-2H20, 2.5 g; nd biotin, 30,ug; in 1 liter of distilled wter. A 5-ml mount of medium ws inoculted with 0.1 ml of 24-h culture nd incubted t 30 C for 48 h. Growth ws mesured in Klett- Summerson colorimeter t 540 nm.
6 ~~~~I 380 NARAYANAN AND RAO ANTIMICROB. AGzNTs CHEMOTHER tl*p.*indolelactic ACID/ O.-,-% 0.4 I4mg/mi wsh 0 E 0 I I I I I p 1.2 _,o9-imdolzetha"cl ' 0.t 0.4i I I I I I I S TIME OF INCUBATION (hr) FIG. 6. Effect of /&lea nd,3ila on growth of C. lbicns. cused by,b-ila my be due to its own effect or The finncil support received by G.R.R. from the Office due to its conversion product. The conversion of of Nvl Reserch, Wshington, D.C., under contrct no. N C-0349, is grtefully cknowledged.,8-ila to (3-IEA is reveled by isolting (8-IEA from culture filtrte of C. lbicns incubted LITERATURE CITED with (8-ILA for 8 h. However, the ntimicrobil effect of (3-ILA by itself is evident from studies on grm-positive nd -negtive orgnisms. Thus, the utontibiotic effect of A3-ILA might be due to its conversion product but my lso be considered s its own effect. The dt presented revel the bility of Cndid spp. to convert norml metbolite such s L-tryptophn to IEA nd (8-ILA. They (3- re possibly biosynthesized vi the following pthwy: L-Tryptophn -+ indole pyruvic cid zt indolelctic cid I indole cetldehyde indoleethnol -- The differences in the quntittive production of vrious lcohols from the corresponding mino cids my be due to the substrte specificity ofthe enzyme nd/or to the utoinhibition exerted by the end products, nmely, the lcohols concerned. ACKNOWLEDGMENTS We thnk M. Sirsi, T. R. Ksturi (Deprtment of Orgnic Chemistry), V. S. R. Ro (Moleculr Biophysics Unit) for helpful discussions. 1. Biley, G. B., nd A. C. Gentile Indole compounds synthesized by Diplodi ntlensis. Plnt Physiol. 37: Duornikov, T. P., G. K. Skrybin, nd N. N. Surorov Tryptmine conversion by Aspergillus niger. (In Russin) Microbiology 37: Kper, J. M., nd H. Veldstr On the metbolism of tryptophn by Agrobcterium tumefciens. Biochim. Biophys. Act 30: Lrsen, P., A. Hrbo., S. Klungsoeyr, nd T. Asheim On the biogenesis of some indole compounds in Acetobcter xylinum. Physiol. Plnt. 15: Lingpp, B. T., M. Prsd, Y. Lingpp, 0. F. Hunt, nd K. Biemnn Phenethyl lcohol nd tryptophol: uto-ntibiotics produced by the fungus Cndid lbicns. Science 163: Nrynn, T. K., nd G. Rmnnd Ro Phenethyl lcohol nd its effect on Cndid species. Proc. Soc. Biol. Chem. Indi 31: Nrynn, T. K., nd G. Rmnnd Ro Phenethyl lcohol nd 2-phenyllctic cid production in Cndid species. Biochem. Biophys. Res. Commun. 58: Rigud, J Synthese d'cide indolyl-3 lctique et de tryptophol pr Rhizobium cultive en presence de tryptophne. C.R. Acd. Sci. 262: Rigud, J L'cide inolyl-3 lctique et son metbolisme chez Rhizohium. Arch. Mikrobiol. 72:
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