A tentative direct microscopic method for counting living marine bacteria.

A tentative direct microscopic method for counting living marine bacteria

Can. J. Microbiol. Downloaded from www.nrcresearchpress.com by UNIV OF WISC MADISON on 04/02/13 For personal use only.

KAZUHIRO KOGURE,USHIOS I M I D U ,A N D NOBUOTAGA Ocetr~rRcsetrrch I~rstitrrtr,U~ril~c~r~.sity (:/'Tokyo,Noktr~ro.7bkyo 164, Jtrl)o~r Accepted December 13. 1978 KOCUKE. K., U. S I M I D U ,N. : ~TACA. ~ ~ 1979. A tentative direct microhcopic method forcounting living marine bacteria. Can. J . Microbial. 25: 415-420. Yeast extract (0.025%) and nulidixic acid (0.002%) were added to seawater samples and the samples were incub;~tedfor6 h at 20°C in thedark. Under these conditions, bacterial celisdid not divide but grew to form elongated cells that are easily recognized by a direct microscopic method and epifluorescent microscopic technique. The number of cells thus obtained is proposed 21s a direct count of viable bacterial cells (DVC). With open ocean saniples. DVC was higher than 'viable' plate counts by LIPto three orders of magnitude and lower than the clirect counts by ~tbout one orde~.. KOGUKE, K., U. S I M I I ) et U N. TACA.1979. A tentative direct microscopic method forcounting living marine bacteria. Can. J . Microbial. 25: 415-420. DesCchantillons d'eau nier ;iuxquels furent ajoutes tle I'extrait tle levure (0.025%) et de I'acide nalidixique (0.002%) furent incubes dulant 6h. sans 1~11nie1.e. :I 20°C. SOLIS ces conrlitions les cellules bacteriennes ne se divisent pas, maiselles font une croissance qui ieurconfere une forme allongee, ce qui les rend facilement reconnaissnbles par les methodes d'examens microscopiq~~es directs et par les techniques microscopiques de I'epifluorescence. Le nornbre de cellules ainsi obtenu est propose conime etant Lrn compte direct des cellules bi~cteriennesviables (DVC). A partir d'echantillons pris dans I'ocean. le DVC est trois fois plus eleve que les comptes de 'viables' fait sur plaques, niais il est une foia moins eleve que les comptes faits par examens directs. [Traduit par Iejourn:~l]

Introduction In marine microbiology the vast differences in bacterial numbers enumerated by direct microscopic counts and by the agar-plate method have been shown by many wol-kers (Jannasch and Jones 1959). Although the differences can be partly attributable to the clumping of cells, dead organisms, and non-living particles in the seawater samples, it is obvious that the viable plate count considerably underestimates the bacterial cells actually living in natur-al seawaters. On the other hand, because of the failure to distinguish living cells from dead ones or from non-living particles, the direct count may result in an overestimation of the viable cells present (Pornel-oy and Johannes 1968; Wiebe and Pomeroy 1972). In the open sea the viable count by the agar-plate method is ~isunllyless than 0.1% of the direct count. In the present report we propose a new method for estimating the viable bacterial numbel-s in seawater by a direct mict.oscopic method. The method involves preincubation of the seawater sample with small amounts of yeast extract and nalidixic acid. Although nalidixic acid, which is a specific inhibitor of DNA synthesis (Goss et 0 1 . 1964), prevents cell division of GI-am-negativebacteria, other synthetic pathways continue to operate, which result in the fol-mation of elongated filamentous cells. This

elongation makes it easier to count cell numbers with the microscope. Presumably beca~lseof the abundance of cellular RNA, acridine orange stained bacteria growing at high I-ateswill fluoresce red orange under the fluorescent micl-oscope. In contrast, inactive bacteria which are poor in cellular RNA, fluoresce greenish white (Daley and Hobbie 1975; Hobbie er trl. 1977). Materials and Methods Lnbortrto,:\ Strrdies Or~rr~ri.s~rr trlrcl Prcl)trrtrtio~r.s P.scrrt/o~rro~rtr.s sp. 108 was isol;~tedin July in 1977 at 28'28' N , 13618' E. in the Northwestern Pacific Ocean dusing the KH77-2 cruise of R/V Iftrkrrho-Morrr (Ocean Research Institute, University of Tokyo). This strain was identified as P.serrt/orrro~rcr.ssp. according to the scheme of Siniidu (1974). P.sercc1o1rro1rtr.s108 was prec~lltul-edin Ili strength of ZoBell's 2216E medi~~ni (Oppenheinier and ZoBell 1952) for 20 h. centrifuged, washed twice with sterile 1.5%. NnCI solution. and inocul~~ted either directly into the culture medium or into the hynthetic salt niixturc (Novitsky and Morita 1976). Cells WCIT kept under starved conditions in this mixture for4 weeksat 20°C before expel.iment;ll use. Gron~tlrC'o1rc1itio11.s For the experimental culture. age!etl seawater was filterecl thl.ough 0.2-pm pore size Nuclepore filters. autoclaved at 121°C for 15min. and enriched with yeast extract (YE) (Difco) and nalidixic acid (NA) (Sigma) :isepticolly. NA was dissolved in before 0.05 N NnOH solution and filter-sterilized ininiedi>~tely use. After the inoculation of the culture, duplicates of200mL

0008-4 166/79/030415-061i;O1.0010 a 1 9 7 9 N:~tionnlResearch Council of Canadu/Conseil national de recherche5 du Canada

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enriched seawater medium were incuhk~teclin 300mL Erlenrnevel. flasks with cotton p l ~ ~ pat s ,2VC for 7 h.

I l c ~ / o ~ r r r i r r t r i i o , (!/' r Direc,/ Cortrrc f I1k")

(!/' Viohlc Btrc~rr~.itrl C~ll.~

For rhe determinarion of DVC, duplicate I(M)-lnL seawater D t ~ ~ o ~ ~ ~ ~t~j'Boc~~er~itrl i i ~ r o ~ i oNrrr~rht~r. ~r samples were enriched with 0.025% ( W / V ) Y E :inel 0.002% B;rclerial growth was followed hy the spre;rcl plate methocl on ( W / V ) N A , and incuh:~tecl in dnl-kness in 250-1111>glass bottles PPES-I1 medium (.raga 1968) ancl ;I clil-ect niicroscopic method. \s with cotton plugs ;it 20°C. A f t e r 6 h o f incubation. ~ ~ n l cotherColonies on cluplic;~teplates were co~rnteclafter 3 days' incubawise statecl, the D V C in the cultureel seawater were determineel tion at 2O"C. Direct counts were obtained sing the e p i f l ~ ~ o r - by the epifluol.escent technique. Only those p;~rticlesthat were escent microscopic method (Hohhie 01 (11. 1977). After 21 preelong;rted 01'fattened to the size ancl shape of freshly culturetl clete~.rninedincubation pe~.iod,a portion of culture nieclium was cells. and that Ruo~.escedreddish orange. were counted. Countfisetl with fol-malin (final concentlxtion 2.0Si). The cells were ing~ were performeel within 5 min after prcpa~.ntion,Before the then fillel-eel onto a 0.2-prn pore size Nuclepol-e filter. The lilter determination o f DVC. the corresponcling T D C s;~mple was wasstained with:rcrieline orange (AO)(Mel.ck. 0.01%) for3 niin. obse~.vecl. I f there were non-hacte~.ialorange-fl~~orescent partiThe filter had previously been so;~kedin 0.2% Nig~.osinsolution cles in the seaw:rte~.. those ~iumherswere counteel and suhfor 10 to20h fo~.obtainingdarker hackground un~lelthe fluorestracteel as a blank from D V C n~~rnbe~.s. cent microscope. After w;~shingwith clistillecl water. the damp filter w;is placed hetweeii a microscope slide ancl a coverslip Results using immel.sion oil (Nikon). All the reagents ( formalin. AO. and elistilled water) ~~secl had p~.eviouslybeen filtel.ed through0.2-[~m Llr Doi.trtoi;~5tri~lie.s pore size Nuclepore filter to eliminate the suspendeel pal.ticlcs. &ff~)c.t of N A 0 1 1 Btrc.toricr1G~.o\~ttll ill E.rpo/le/rtirll A Nikon fluorescent microscope with an ultr;i-high mercury Pl11rsc. I;uiip w a j ~ ~ s efor c l the observiition o f the prep;~t.;~tionsat x 1000 Actively growing bacterial cells were inoculated m;~gnification.B-B excitation filtel-s ancl 21 Y-SON F ha~.rie~. filter we!-e usecl. The numbel. o f b>rcte~.ia pel- rnillilitre were estimated into seawater medi~imenriched with 0.025% YE l l y than 300cells. All from :Icount ofiit least 200 cells, ~ ~ s u ; ~more and various concentrations of NA. Twenty or pal-ticles were counted as total direct counts the b;~cte~.i;~-like thirty milligrams/L NA (0.002% or 0.003%) inhib(TDC). Those cells elongated or enlarged to the size o f freshly ited bacterial division such that the total direct cultul-ed bactel-ia were counted and designateel ;IS direct counts i : ~ l ( D V C ) . Blank tests were irlso carried out o f viable b ~ ~ c t e r cells counts did not increase (Fig. 2B), and plate counts without the sample se;lwater. decreased m:u-kedly (Fig. 2A). At I0 mg/L NA. the Fieltl Sirtt1ic.s Sctr n,olt,r Strr,rplirrg.s Seaw;itcrsarnplings were made in December, 1977. at stations in or near the Kuroshio Ci11.1.entduring the KH-77-4 cruise o f R/V Htrklrlro-Mtrrrc (Fig. I).Samples were collected with sterilizeel J-Z type O R l T samplers (Taga 1968) or sterilized glklss bottles for s~rrfilcelayers. All the microhiologic;~l treatments were done within 1 h on hoard. 11c~lt~1~rrrir~trlit111 t~/'Pltrlc Corrrrl (PC) t r r ~ t l7i110l Iliroc~lCorrrrl (71)C) For the enumeration o f heterotrophic h~lcteria,appropriate amounts (1-50mL) o f duplicate seawater stlmples were filtered through 0.2-pm pore size Nuclepore filters. The inoculated filters were put on PPES-I1 agar plates ancl then incubated at 20°C for3 weeks before countingcolonies. T D C was determined by the srme epifluorescent technique 21s rnentioncd above. All the bacteria-like particles which have clear margins and greenish white or orange fluorescence were counted. At least 400 cells were counted for each preparation.

total direct count gradually increased, which indicates that this concentration was insufficient for the complete inhibition of bacterial tlivisions. Cell elongation during the incubation period was also determined with at least 20 cells (Fig. 3). In the presence of20 mg/L NA and aftel-7 hof incubation, ~ ttimes the length of those the cells reached a b o ~ 10 without NA. The addition of 20 mg/L of N A suppressed bacteI-ial division despite varying the concentration of YEfl-om 0.0002 to0.025% (data not shown). During the course of incubation, all the bacterial cells counted as TDC fluoresced reddish orange.

121 Pacific Ocean

5

0 Time th) FIG. 1. Sampling locations during KH-77-4 cruise of RIV Htrklrllo-Mtrrlr.

0 Time

5 th)

FIG. 2. Growth o f P.~c.rrtlor,lot~trs108 with various concentrations of nalidixic acid. ( A ) PC, (B) TDC.


KOGURE

0

5 Time t h )

FIG.3 Change in cell length of P\errt/oti~ot~tr( 108 during the of incutx~t~on. Clo\ed circle\: with 0.002% (20 rngll.) nnlldixic ncld; open circle\: wltho~ltnalldlx~c;~cid.

caul \e

Efic.r of N A otl rlre Gro~t>rlr oJ'Stnt.oerl Brrcrerin Bacterial cells that had been kept ina salt mixt~11.e for 4 weeks were inoculated into the seawater medium enriched with 0.025% Y E and 0.002% (20mgIL) NA (Fig. 4). Through the incubation period (Fig. 4), the plate counts were about 15% of direct counts. During the lag phase, which continued for 5 h, the direct count and plate count neither increased nor decreased, regardless of the presence of NA. This indicates that it is not until the beginning of exponential growth phase that the bactericidal action of NA emerges and the viability decreases. In the PI esence of NA, the direct counts remained constant during the incubation period. After 5 h of incubation, some of the cells greatly enlarged and fluoresced reddish orange. These appeared to be living bacterial cells, whereas the remainder did not show any morphological changes and fluoresced greenish white. The latter were t h o ~ ~ gto h t be dead cells. o r at leajt those unable to recover their viability under the present culture condition. At time 0, the mean size of the starved bacteria wa5 0.61tni and aftel- 5 h, the size of elongated cell5 wa5 3 01.4pni. The ~.atiosof the enlarged living cells (DVC) to total direct count (TDC) are 4hown in Fig. 5. Although the enlarged cells increased with incubation period, the difference between the presence or absence of NA i5 clear. In the presence of NA, the number of enlarged cell5 became constant at 5 h. and their ratio to TDC did not exceed one-third. Without NA, the vigorous bacterial fissions were reflected in the con5tant increase in the ratio. The above result\ \bowed that after- 4 week5 5ta1vat ion, 33% of TDC col-responds to DVC and 15% to PC.

F I G .4. C~.owlhof stal-vecl P.serrtlot~roirrr.s108. Ciscleh: with 0.002% (?Omg/L) nalidixic acid; triangles: without nalidixic acid.

801

0

5 Time ( h )

FIG.5 . K:~tioofDVC to total direct count during the cousse of 108. Closed circles: with O.OO?%> incubation of P.ct~rctlo~~ro/ro.v nalidixic acid: open circle\: without nalidixic acid.

h-ic~ldsrrrrtic.\ lZf7i.c.r (!I' N A otl Bac.rcria1 Gt.o~~,rll it1 N t r t r l t ~ ~ l Sccr\~wter Surface water collected at Station P (Fig. 1) was incubated up to 1 1 h and PC and DVC in the water were determined during the course of the incubation (Fig. 6). With the addition of 0.002% NA. the cell divisions wer-e suppressed at least up to 5 h. This suggests that NA may also be effective on natural heterogeneous bacterial populations. After 5 h of incubation, the bacterial cells which were counted as DVC swelled to about 1 pni and

C A N . J . MICROBIOL. VOL. 25. 1979

Bacteria

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t DV C

TDC d

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FIL 6. G ~ o w t hof h ' t c t e ~ ~Ina n n t u ~ a l\earv,ttel. C ~ ~ c l ewith \ 0.002% nCilidivlc'~clcl;t~ angle\. wlthout nulid~\ic,~cld.

~1

I

TDC

200

I

1 '

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FIG.8. Vertical plufiles of bacteria. (A) Station 153. ( B ) Station 49. (C) Station 121.

fluol-esced reddish orange. Thl-ee hours' incubation was insufficient for clear differential counting of fattened cells. Unclel- the growth conditions used, 5 or 6 h of incubation was best for the determination of DVC. Vertic,nl Profiles of Btrctericr ill Operz Ocerirl

Time ( h FIG.7. DVC changes during the course of seawater incubations collected at Station 153. Closed circles: O m ; open circles: I0 rn: squares: jOrn; closed triangles: 100 rn; open triangles: 200 m.

At Station 153, the seawater samples collected at 0, 10, 50, 100, and 200 m depth were incubated for 8 h and DVC were followed (Fig. 7). The differences between DVC values after 5 and 6h of incubation were small. Although either incubation time could be used, the latter was chosen to measure DVC in natural seawater, since the enlargement of the cells at 6 h was clearer than at 5 h. Figure 8A, B, and C show the vertical profiles of PC, DVC, and TDC at Stations 153, 49, and 121, I-espectively. PC values were roughly 0.1% of DVC, which were

419

KOGURE ET A L .


about 5-10% of TDC. In natul-al seawater, all the bacteria counted as TDC were small in size (about 0.3 pin) and large cleat-ly living bacterial cells which fluoi-esced reddish orange were not detected.

Discussion The present ~'es~tltsshowed that the DVC niethod may provide a useful technique for counting bacterial numbers in natural seawaters. With this technique, only living cells can be detected, which was impossible by conventional direct microscopic method\. The procedure is I-elatively simple and the results can be obtained within a short period of time. In the label-atory experiments, Pserrtioinoi7cl~ 108 was sensitive to the bactericidal action of NA at a concentration of0.002% or mole, which led to the fol-niation of elongated filamentous cells. Goss et (11. (1964) described the same effect ofNA on E. coli and further observed that NA was lethal only for proliferating cells. Deitz el (11. ( 1966) stated that protein and ribonucleic acid synthesis were PI-erequisites for the bactel-icidal action of NA. These observations are consistent with the fact that bactericidal action of NA on P J P I I ( / ~ I ? ~ 108 O I ~be(IJ came apparent after the beginning of the exponential growth phase. These charactel-istics of NA favout- the present technique. The growth of natut al bacterial population, however, could not be completely suppressed by NA. Even with a highel-concentration of NA, it wa\ also impossible to inhibit the bacterial division (data not shown). This must be due to growth of NAI esistant bacteria. The role of NA in this technique is to retard the beginning of the exponential growth phase for at least 6 h and avoid the overestimation of living cells. The incubation pl.ocedure of seawater samples, couplecl with the use of the epifluol-escence technique with acl idine orange staining, greatly eased the discl-imination of living cells from other particles. Several investigators have reported the presence of many small. free-living, coccoid bacteria in natural seawater (Daley and Hobbie 1975; Watson et (11. 1977; Zirnmermann ancl Meyer-Reil 1974). Most of them fluoresced greenish white, whereas the cultured cells fluoresced reddish orange. Hobbie et (11. (1977) have suggested that this may be the I-esultof interaction between cellula~-RNA and acridine orange. If so, this difference in fluorescence colour makes it easier to count only living cell5 as DVC. Just after the A 0 staining, all the swollen bactet-i'~Icells fluoresced reddish orange, but a part of non-swollen particles sometimes aluo fluoresced

reddish orange. Longer staining time or higher A 0 concentration often resulted in such non-soecific orange fl~lorescence.Those pat-ticles which did not show cleat- bacterial morphology were not counted as DVC. Once the prepat-ations were exposed to near ultraviolet radiation, the reddish-orange colour began to fade, and aftel-that only greenish white fluol-escence remained. As fol. the large swollen cells, the reddish-orange fluorescence lasted longer than that of non-swollen small particles. Significant differences were seen bet ween TDC, DVC, ancl PC values after4 weeks' starvation and still greatel- differences were found with natural seawater samples. The differences between TDC and DVC could be mostly asct-ibetl to dead organisms or non-living particles. T o confirm this assumption. further experiments with various antibnctet-ial acents and under different conditions of incubation will be necessary. There may be other better antibacterial agents or their appropriate combinations that effectivelv inhibit cell division. Further investigations on nutrient conditions which favour the growth of more bacterial cells will be also required. Particular emphasis should be given to the concentl.ation of nutrients with the view to the prevalence of oligotl.ophic bacterial populations in the open sea. While all the par-ticles which did not enlarge during the incubation period under the present expel-imental condition may not necessarily be dead organisms, the elongated cells were obviously living bacterial cells. The met hod is thus PI-obablya minimum estimate of viable cell numbers. Nevertheless the number of living bacteria counted with this method was f a - greater than any other previous method of counting living bacteria in the sea. Microscopic observation clal.ities some aspects of bacterial life in natural seawaters. Most cells counted as TDC were small coccoid forms, about 0.3pm in cliarneter. On the other hand, most cells counted as DVC were free-living; about 70% of were still them were rod-shaped, but the ~.eniaindetcoccoid. It is not certain whether these cells will become rod-shaped after longer incubation. These coccoitl cells tended to make clumps. On the other hand, most of detrital particles did not contain detectable bacterial cells on the surfaces. However, flakes (Gordon 1970) were often found to have some bacterial cells attached on the surface. As a consequence, this counting technique (DVC) may prove to be very useful and valuable as a new counting method. Further impt-ovementsand applications to various environments will be necessary in the future.

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Acknowledgment Grateful acknowletlgnient is expressed to Dr. R. Y . Morita, Department of Miclubiology and School of Oceanography, Oregon State University, for kind rentling and criticizing of this manuscript. Gratitude is clue to Dr. T . Kume, Ocean Research Institute, University of Tokyo, for his suggestion and encouragenient for the study. We also thank the officers and crew of R/V HrrXnIzo-Mtr1.11for help in collecting and treating seawater samples. DALEY. K. J.. and J . E. H O B B I E1975. . Direct count of :tqu>ttic bacteria by a modified epifluorescent technique. Lirnnol. Oceatiogr. 20: 875-88 1. 1 1 ~ 1 - I ZW. , H.. T. M. COOK.itnd W. A. GOSS.1966. Mechanism of action of nalidixic acid on E.vclreric.lritr coli. 111. Conditions requiretl for lethality. J . Bacteriol. 91: 768-773. GORDON, D. C . . JIG. 1970. A microscopic study of organic particles in the North Atlantic Ocean. Deep-Sea Kes. 17: 175-185. Goss. W. A,. W . H . DEITZ,and T. M. COOK.1964. Mechanism coli. J . Bacteriol. 88: of action of nalidixic acid on E.sclrc~~.iclricr 1112-1118. HOBBIE J ., E., R. J. DALLY,and S. JASPER. 1977. Use of Nuclepore filters for counting hactel-ia by fluorescence micr-oscopy. Appl. Environ. Microbiol. 33: 1225- 1228. JANNASCH. H. W.,itnd G. E. JONES.1959. Bacterial populations

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