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J= OURNAL OF CULTURE COLLECTIONS

Volume 5, 20= 06-2007, pp. 78-84

 

 

 

DIVERSITY OF BACILLUS GENOTYPES IN SOIL S= AMPLES FROM

EL-OMAYED BIOSPHERE RESERVE IN EGYPT

 

Eman A. H. Mohamed1, Mikiko Abe2, Khaled M. Ghanem1, Yasser R. Abdel-Fattah3,
Yasuyoshi Nakagawa4 and Ehab R. El-Hel= ow1*

 

1Department of Botany, Faculty of Science, University of Alexandria, Alexandria, Egypt;=
2Department = of Chemistry and BioScience, Faculty of Science, Kagoshima University, Kagoshi= ma 890-0065, Japan;
3Department = of Bioprocess Development, Genetic Engineering and Biotechnology Research Institute, Alexandria, Egypt; <= br> 4Biological = Resource Center, National Institute of Technology and Evaluation, Kisarazu 2920818, Japan

*Corresponding author, e-mail: elhelow@link.net

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Summary

Sequencing of the 1= 6S rDNA hypervariant region was applied to determine the presence and composition o= f Bacillus species in 40 soil sam= ples randomly collected from different habitats in El-Omayed biosphere reserve, = Egypt. = Although purified cultures showed 18 different phenotypes that were morphologically distinct on a sporulation medium plate, only 4 different nucleotide sequenc= es designated Seq A, B, C and D were revealed. Computational ana= lysis of DNA sequence data suggested that 17 of these isolates are closely related members of the Bacillus <= span style=3D'mso-bidi-font-style:italic'>cereus/thuringiensis group (Seq= B, C and D) and one isolate is belonging to the Bacillus subtilis group (Seq A). Further phenotyp= ic investigations confirmed the diversity of the 17 novel Bacillus cereus/t= huringiensis isolates and indicated that the new Bacillus subtilis group isolate is a Bacillus amyloliquefaciens strain. A simple phenotypic discrimination key that can be applied for distinguishing between such closely related Bacillus cereus/thuringiensis m= embers is presented.

Key words: Bacillus amyloliquefaciens; Bacillus cereus= ; Bacillus thuringiensis; spore formers; 16S rDNA

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Introduction

Soil is the main reservoir of the genus Bacillus [26]. Members of this genus are used for the synthesis of a very wide range of important medical, agricultural, pharmaceutical and other industrial produc= ts. These include a variety of antibiotics, enzymes, amino acids and sugars [11= ].

Sequencing of the 16S rDNA hypervariant region (ap= prox 275 bp close to the 5’ end region) is a rapid and reliable way for Bacillus classification = and basically informative at species level [4]. Nevertheless, full sequencing of the16S rDNA gene is sometimes useful for more detailed classification within some Bacillus groups. On the other hand, closely related taxa are of= ten extremely similar in their 16S rDNA sequences [13]. For instance, some memb= ers of the Bacillus cereus group (B. anthracis, B. cereus and = B. thuringiensis) have high levels of 16S rDNA sequence similarity (>99 %) [21].

However, some phenotypic characters such as β-hemolytic activity can be used to distinguish between B. cer= eus and B. thuringiensis on the one hand and B. anthracis on the other hand [5, 14, 20].

The main objective of the present work is to explo= re the presence and composition of Bacillus species in representative soil samples collected from El-Omayed biosphere reserve in Egypt. = Eighteen different spore forming bacterial strains were isolated, characterized and identified at the molecular level. A discrimination key for distinguishing between closely related individual members is presented.

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Materials and Methods

Bacterial isolation. The study a= rea, El-Omayed biosphere reserve, is a part of the northwestern Mediterranean coastal zone of Egypt [8]. Forty soil samples were collected from five natu= ral habitat types, including coastal dunes, inland ridges with skeletal shallow soils, saline marshy depressions, non-saline depressions and inland plateau= . In all cases, soil samples were taken from 2 to 5 cm layers. A gram of= each well-mixed sample was suspended in 50 ml of 2 x SG sporulation medium [23], then incubated at 37 oC under shaking conditions (200 rpm) for 48 h. Vegetative cells were killed by adding chloroform (1 % v/v), vortexing and keeping for 24 h at room temperature. Spores were germinated by plating 0.1 ml of each spore suspension with and with-out dilutions, into solidified 2 x SG medium. Isolated colonies were further purified by streaking on agar plates of the same medium.

Reference strains. B. cereus<= /span> 4F1 and B. thuringiensis 4A1 were obtained from <= st1:PlaceName w:st=3D"on">Bacillus Gene= tic Stock Center (BGSC), Ohio State University, Columbus, OH, U.S.= A. B. amyloliquefaciens 23350 was obtained from American Type Cult= ure Collection (ATCC) and B. subtilis 3007 was obtained from= the Institute for Fermentation, Osaka (IFO), Japan.

Phenotypic analyses. Pure cultur= es were examined for motility, Gram reaction, spore morphology, Voges-Prauskauer te= st, citrate utilization, nitrate reduction, β-hemolytic activity, catalase= and oxidase expression and production of acids from D-glucose, L-arabinose, D-xylose and D-mannitol [5, 2, 24]. The expression of some other enzymes such as β-glucosidase and N-acetyl-β-glucosaminidase was = also examined in addition to the ability to degrade Tween 80, gelatin, case= in, chitin, starch, pectin xylan and mannan [9, 18]. Fatty acid profiles were determined using the method described by Sasser [22].

DNA preparation and PCR amplification. Bacterial cells were obtained from late-exponential cultures shaken in LB medium at 37 oC. Genomic DNA of Bacillus strains was prepared for PCR amplification [25] and the primers used for PCR and sequen= cing are shown in Table 1. The primers 16S-1 and 16S-2 were used to amplify= a fragment of about 270 bp that inclu-des the 16S rDNA hypervariant region [2= 7]. F9 and R1510 primers were used to fully amplify the 16S rDNA gene. F9, F515, F785, F1099, R1510, R1115, R802 and R536 were separately used for DNA sequencing. The PCR reac- tion mixture contained 200 μM of each dNTP, = 0.5 μM primers, 10 mM= tris-HCl pH 8.3, 1.5 mM MgCl2, 50 mM KCl, 2.5 U Taq polymerase and about 100 ng of template DNA. For 16S-1 and 16S-2, amplicons were obtained with a PCR cycling program of 94 oC for 5 min, 30 cycles = at 94 oC for 30 s, 55 oC for 30 s and 72 = oC for 30 s. At the end, the reaction was incubated at 72 oC f= or 7 min. For F9 and R1510, the cycling program was 95 oC for 3 = min, 30 cycles at 95 oC for 30 s, 55 oC for 15 s= and 72 oC for 1 min and at the end, the reaction was incub= ated at 72 oC for 5 min. Amplicons were visualized by electrophoretic separation on 2 % agarose gels stain-ed with ethidium bromide.

 

Table 1. Primers specific for 16S rDNA.

Primer

Sequence (5` to 3`)

16S-11

TGGCTCAGAACGAACGCTGGCGGC

16S-21

CCCACTGCTGCCTCCCGTAGGAGT

F92

GAGTTTGATCCTGGCTCAG

F5152

GTGCCAGCAGCCGCGGT

F7852

GGATTAGATACCCTGGTAGTC

F10992

GCAACGAGCGCAACCC

R15102

GGCTACCTTGTTACGA

R11152

AGGGTTGCGCTCGTTG

R8022

TACCAGGGTATCTAATCC

R5362

GTATTACCGCGGCTGCTG

Note: 1According [27]; 2 Department of Biochemistry and Bioscience,

Faculty of Science, Kagoshima University, Japan.

 

DNA sequencing and data analysis. PCR fragments were purified by QIAquick PCR purification reagents (Qiagen), lab= eled with Big Dye Terminator Cycle Sequencing Kit and DNA sequences were obtained using ABI PRISM 310 sequencer (Perkin Elmer, Applied Biosystem, USA). Homol= ogy search was performed against DDBJ (DNA Data Base Japan) using Blast program. Multisequence alignment and molecular phylogeny analyses were performed usi= ng ClustalW (a distance-based analysis program). The resulted tree topology was evaluated using bootstrap analysis of the neighbor-joining method based on = 1000 resamplings [3]. All sequences have been deposited in the Gen-bank and their accession numbers are given in Table 2.

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Table 2. Accession numbers of the novel Bacillus soil isolates.

Isolate number

Sequence type

Accession number

EM44

16S rDNA partial sequence

DQ389737

EM62

16S rDNA partial sequence

DQ389738

EM1

16S rDNA partial sequence

DQ389739

EM3

16S rDNA partial sequence

DQ389740

EM4

16S rDNA partial sequence

DQ389741

EM15

16S rDNA partial sequence

DQ389742

EM25

16S rDNA partial sequence

DQ389743

EM33

16S rDNA partial sequence

DQ389744

EM35

16S rDNA partial sequence

DQ389745

EM37

16S rDNA partial sequence

DQ389746

EM42

16S rDNA partial sequence

DQ389747

EM46

16S rDNA partial sequence

DQ389748

EM50

16S rDNA partial sequence

DQ389749

EM52

16S rDNA partial sequence

DQ389750

EM58

16S rDNA partial sequence

DQ389751

EM60

16S rDNA partial sequence

DQ389752

EM63

16S rDNA partial sequence

DQ389753

EM29

16S rDNA partial sequence

DQ389754

EM44

16S rDNA full sequence

DQ389755

 

Results and Discussion

A number of spore-forming bacteria isolated from 40 different = soil samples showed 18 different phenotypes that were morphologically distinct o= n sporulation medium plates. Colony morphology of the isolate EM44 was very unique becaus= e of its wrinkled configuration. All isolates were further purified for molecular and phenotypic characterization. Preliminary results showed that all of the isolates are Gram positive bacilli and form oval spores that do not cause mother cell swelling.

Sequen= cing of the hypervariant region (275 bp) of 16S rDNA [4] in the 18 soil isolates resulted in only 4 different nucleotide sequences designated Seq A, B, C an= d D. Based on theses sequences and their comparative computational analyses, phylogenetic positions of the experimental isolates are shown in Fig. 1. Th= ese results suggested that the isolate EM44, which carries Seq A, is belonging = to the B. subtilis group and that each of the other 17 isolates, which comprise Seq B, C or D is likely a member of the Bacillus cereus/= thuringiensis group.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 


Fig. 1. A phylogenetic tree based on partial sequencing of the 16S rDNA gene. The tree was constructed by neighb= or-joining method using ClustalW software. The scale indicates substitutions per site.= The numbers at the nodes indicate the frequency of occurrence in 1000 bootstrap= ped trees. App.: Seq A, isolate EM44; Seq B, isolate EM62; Seq C, isolat= es EM1, EM3, EM4, EM15, EM25, EM33, EM35, EM37, EM42, EM46, EM50, EM52, EM58, = EM60 and EM63 and Seq D, isolate EM29.

 

For further characterization, the 18 isolates together with representative reference members of the genus Bacillus (B. cereus, B. thuringiensis, B. subtilis an= d B. amyloliquefaciens) were examined with respect to some biochemical and nutritional features. All strains expressed catalase, chitinase and caseina= se. Besides, all of them were able to ferment D-glucose producing stable acidic= end products (positive methyl red test) but not neutral ones (negative Voges-Prauskauer reaction). On the other hand, the utilization of pectin, x= ylan and mannan; fermentation of D-xylose and expression of β-hemolytic activity appeared to be powerful features in differentiation between examin= ed B. cereus and B. subtilis groups (Table 3).

 

Table 3. Phenotypic characteristics of the Bacillus soil isolates.

Isolate

or

strain

Mot

Cit

Nit

β-Hem

Oxd

L-Ara

D-Man

D-Xyl

β-Glu

N-Amn

T-80

Gel

Str

P, X, M

EM1

+

+

-

+

+

-

-

-

+

-

-

+

+

-

EM3

+

+

+

+

+

-

-

-

-

+

+

+

+

-

EM4

-

-

-

+

-

-

-

-

+

-

-

-

+

-

EM15

+

-

+

+

-

-

-

-

+

-

-

+

+

-

EM25

+

-

+

+

+

+

+

-

-

-

+

+

-

-

EM29

+

-

+

+

+

-

-

-

-

-

+

-

+

-

EM33

+

-

+

+

+

-

-

-

-

-

-

+

+

 

EM35

+

+

+

+

-

+

+

-

-

+

+

-

+

-

EM37

+

+

+

+

+

+

+

-

-

-

-

+

+

-

EM42

+

-

-

+

+

-

-

-

-

+

-

+

+

-

EM44

+

+

+

-

-

+

+

+

+

-

+

+

+

+

EM46

+

-

-

+

+

+

+

-

-

-

+

-

+

-

EM50

+

-

+

+

-

-

-

-

-

-

-

+

-

-

EM52

-

-

+

+

+

-

-

-

-

-

+

+

+

-

EM58

+

+

+

+

-

-

-

-

-

-

+

+

+

-

EM60

+

-

-

+

+

-

-

-

-

-

+

+

+

-

EM62

-

-

-

+

+

-

-

-

-

-

-

+

+

-

EM63

+

+

+

+

+

-

-

-

-

-

-

+

+

-

Ba 23350

+

+

-

-

-

+

+

+

+

-

+

+

+

+

Bs 3007

+

-

+

-

+

+

+

+

+

-

+

+

+

+

Bc 4F1

+

+

-

+

-

-

-

-

-

+

-

+

-

-

Bt 4A1

+

-

+

+

-

-

-

-

-

-

+

+

+

-

Legend: motility (Mot), citrate utilization (Cit), nitrate red= uction (Nit), β-hemolysis (= β-Hem), oxidase production (Oxd), acid production from L-arabinose, D-mannit= ol and D-xylose, respectively (L-A= ra, D-Man and D-Xyl), β-glucosidase production (β-Glu), N-acetyl-β-glucoseaminidase productuin (N-Amn= ), utilization of Tween 80 (T-80), gelatin hydrolysis (Gel), starch degradation (Str), degradation of pectin, xylan and mannan, respectively (P, X, M); B. amyloliquefaciens (Ba= ), B. subtilis (Bs), B. cereus (Bc); B. thuringiensis (Bt).

 

Members of the B. cereus group, especially B. anthra= cis, B. cereus and B. thuringiensis, are so closely related to each o= ther that they are treated by some authors as only one species [10, 19, 7, 17]. Likewise, the novel 17 morphologically distinct B. cereus/thur= ingiensis isolates were grouped into only three clusters based on the hypervariant re= gion of the 16S rDNA. According to the results presented in Table 3, a discrimination ke= y is suggested for complete resolution of these closely related isolates. The ability to degrade Tween 80 can divide these isolates into degraders a= nd non-degraders. Then, citrate utilization can subdivide each category into 2 subgroups. Sequential tests including nit-rate reduction, mannitol utilizat= ion, gelatin hydrolyses, N-acetyl-β-glucosaminidase expression, β-glucosidase activity and starch degradation subdivide them further until reaching a full discriminat= ion between the 17 isolates.

The entire new B. cereus strains’ group exhibited chitinase and β-hemolytic activities. In addition, the majority of the= m were motile. The-se results role out for all isolates the possibility of being <= i>B. anthracis [5]. However, further investigations are required for these n= ew isolates that may comprise a variety of B. thuringiensis genotypes, = used as highly specialized and powerful biological agents for controlling insect pests [1, 16].

Generally, the B. subtilis group includes a numb= er of industrially important species which are used in a wide range of industrial applications [2, 6, 15]. Our results suggest a possible industrial importan= ce of the isolate EM44. This strain has the ability to produce a considerable range of extracellular enzymes such as α-amylase, gelatinase, xylanase, mannanase, pectinase and caseinase.

Because of its promising applicable features, isolate EM44 was subjected to further analyses to determine the exact species to which it belongs within the B. subtilis group. Full sequencing of the 16S rDNA gene of the isolate EM44 and its computer database alignment recorded a similarity of 99% to a B. amyloliquefaciens reference strain (F= ig 2.). For further verification whole cell fatty acid composition of isolate EM44, along with reference strains of B. amyloliquefaciens and = B. subtilis (Table 4), was analyzed. The results revealed that the levels of the most d= ominant fatty acids in the cells of isolate EM44 (15:0 Iso and 15:0 Anteiso) are cl= oser to B. amyloliquefaciens rather than to B. subtilis. Moreover, this novel Bacillus strain was clearly characterized by over-express= ion of α-amyl= ase on starch plates (data not shown).

 

 

 

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Fig. 2. Phylogenetic position of isolate EM44 based on full sequencing= of 16S rDNA. The tree constructed by neighbor-joining method using ClustalW so= ftware. The scale indicates substitutions per site. The numbers at the nodes indica= te the frequency of occurrence in 1000 bootstrapped trees.

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Table 4. Fatty acid composition analysis of isolate EM44 <= /span>and two reference strains. <= span lang=3DEN-US>Values are shown as percentages.

Fatty acid

Bacterium

B. amyloliquefac= iens

B. subtilis

EM44

11:0 Iso 3OH=

-

0.11

-

12:00

-

-

0.34

13:0 Iso

0.15

0.67

0.25

13:0 Anteiso=

-

0.16

0.12

14:0 Iso

2.7

1.68

1.57

14:00

0.43

1.51

0.95

15:0 Iso

16.24

31.37

20.01

15:0 Anteiso=

33.57

27.28

33.82

15:00

0.27

0.32

0.22

15:0 Iso 3OH=

-

-

0.42

15:0 2OH

-

-

0.35

16:0 Iso

10.01

4.33

4.37

16:00

5.99

9.03

10.73

17:0 Iso

16.1

16.69

14.81

17:0 Anteiso=

13.39

6.55

11.31

18:00

0.63

0.3

0.72

 

References

1.&n= bsp; Baum, J. A., T. B. Johnson, B. C. Carlton, 1999. Bacillus thuringiensis natural and recombinant bioinsecticide products. In: Methods in Biotechnology, Hall, F. R., J. J. Mean (Eds), Vol 5, Totowa, NJ: Humana Press, Inc., 189–209.

2.&n= bsp; Carr, J. G., 1983. J. Appl. Bacteriol., 55, 383- 402.

3.&n= bsp; Felsenstein, J., 1985. Evolution, 39, 783-791.

4.&n= bsp; Goto, K., T. Omura, Y. Hara, Y. Sadaie, 2000. J. Gen. = Appl. Microbiol., 46, 1-8.

5.&n= bsp; Guttmann, D. M., D. J. Ellar, 2000. FEMS Microbiol. Lett.,<= /i> 188, 7-13.

6.&n= bsp; Hara, T., S. Veda, 1982. Agricul. Biol. Chem., 29, 45-72.

7.&n= bsp; Helgason, E., O. A. Okstad, H. A. Johansen, A. Fouet, M. Mock,= 2000. Appl. Environ. Microbiol., 66, 2627-2630.

8.&n= bsp; Ismail, H. A., S. M. H. Abd El-Rahman, F. H. Abdel-Kade= r, 1986. Cah. Orstom., ser. Pedol., XXII, 63-76.

9.&n= bsp; Ivanova, E. P., V. V. Mikhail, V. I. Sventashiv, O. I. Nedashkovskayan, N. M. Gorshkova, V. V. Mikhailov, N. Yumoto, Y. Shigeri, T. Taguchi, S. Yoshikawa, 1999. Internatl. Microbiol., 2, 267-271.

10.&= nbsp; Jensen, B. G., N. Fisker, T. Sparso, L. Andrup, 2005. Inter= natl. J. Food Microbiol., 104, 113-120.

11.&= nbsp; Joung, K. B., J.-C. Cote, 2002. J. Appl. Microbiol., 92, 97-108.

12.&= nbsp; Koneman, E. W., S. D. Allen, W. M. Janda, P. C. Schreckenberger, W. C. Winn, 1992. Diagnostic Microbiology, 4th<= /sup> edn, Philadelphia, = Pa: J. B. Lippincott Co.

13.&= nbsp; La-Duc, M. T., M. Satomi, N. Agata, K. Venkateswaran, 2004. J. Microbiol. Meth., 56, 383-394.

14.&= nbsp; Mabuchi, N., I. Hashizume, = Y. Araki, 2000. Can.= J. Microbiol., 46, 370-375.

15.&= nbsp; Parry, J. M., P. C. B Turnbull, J. R. Gibson, 1983. A Color Atlas of Bacillus Species, Ipswich: Wolfe Medical Publications ltd.

16.&= nbsp; Pena, G., J. Miranda-Rios, G. de la Riva, L. Par-do-Lopez, M. Soberno, A. Bravo, 2006. Appl. Environ. Microbiol., 72 (1), 353-360.

17.&= nbsp; Peter, T. C. B., P. J. Jackson, K. Hill, P. Kein, A.-B. Kolsto= , D. J. Beecher, 2002. Long standing taxonomic enigmas within the Bacillus ce= reus group are on the verge of being resolved by far-reaching molecular developments: Fore-casts on the possible out come by an ad hoc team. In: Applications and Systematics of Bacillus and Relatives, Berkeley, R., M. Heyndrickx, N. Logan, P. De Vas (Ed= s), Oxford: Blackwell Publishing, 23-36.

18.&= nbsp; Pirttijarvi, T. S. M., M. A. Andersson, M. S. Salkinoja-Salone= n, 2000. Internatl. J. Food Microbiol., 60, 231-239.

19.&= nbsp; Rasko, D. A., M. R. Altherr, C. S. Han, J. Ravel, 2005. FEMS Microbiol. Rev., 29, 303-329.

20.&= nbsp; Rhodenhamel, E. J., S. M. Harmon, 2001. Bacillus cereus. In: Ba= cteriological Analytical Manual, Belay, N., D. B. Shah, R. Bennett (Eds), 8th edn, USA: FDA, Center of Food Safe= ty and Applied Nutrition.

21.&= nbsp; Sacchi, C. T., A. M. Whitney, L. W. Mayer, R. Morey, A. Steige= rwalt, A. Boras, R. S. Weyant, T. Popovic, 2002. Emerg. Infec. Dis., 8,<= /b> 1117- 1123.

22.&= nbsp; Sasser, M., 1990. Identification of bacteria through fatty acid analysis. In: Methods in Phytobacteriology, Klem= ent, Z., K. Rudolph, D. C. Sands (Eds), Budapest: Akademiai, Kiado, 900-911.

23.&= nbsp; Schaeffer, P., 1969. Bacteriol. Rev., 33, 201-204.

24.&= nbsp; Sneath, P. A., N. S. Mair, M. E. Sharphe= , 1986. Bergey`s manual of systematic bacteriology, vol. 2, Baltimore, London, = Los. Angeles, Sidney: William and Wilkins.

25.&= nbsp; Wang, S., S. Wu, G. Thottappilly, R. D. Locy, N. K. Singh, 2001. J. Biosc. Bioengin., 92, 59-66.

26.&= nbsp; Watanabe, K., K. Hayano, 1993. <= st1:country-region w:st=3D"on">Can. J. Microbiol.<= /i>, 39, 674-680.

27.&= nbsp; Young, J. P. W., H. L. Downer, B. D. Eardly, 1991. J= . Bacteriol., 173, 2271-2277.

 

 

 

РАЗН&#= 1054;ОБРАЗИЕ НА ГЕНОТИПОВЕ BACILLUS= В ПОЧВЕНИ ПРОБИ
ОТ БИОСФЕРНИЯ РЕЗЕРВАТ EL-OMAYED= = В ЕГИПЕТ

 

Еман А. Х= ;. Мохамед1, Микико Абе2, Калед М. Джанем1, Ясер Р. Абдел-Фатах3,

Ясуйош&#= 1080; Накагава4, Ехаб Р. Ел-Хелоу1*<= /span>

 

= Резюме

&= #1055;риложено е секвенира = 85;е на хипервариаl= 5;тната област на 16S рДНК за определяне присъствиеm= 0;о и състава на вида Bacillus = в 40 почвени проби, събрани случайно от различни местообитаl= 5;ия в биосферни = 03; резерват El-Omayed= , Египет. Въпреки че пречистениm= 0;е култури пок = 72;зват 18 различни фенотипа, които се разграничаk= 4;ат морфологичl= 5;о на среда за спорулация, са открити само 4 различни нуклеотиднl= 0; последоватk= 7;лности, означени като Seq A, B, C и D. Компютърниn= 3;т анализ на данните от ДНК секвени = 88;ането предполага, че 17 от тези изолати са т= 103;сно родствени членове на групата Bacillus cereus/thuringiensis (Seq B, C и D),= а един изолат принадлежи към групата Bacillus subt= ilis = (Seq A)= . Понататъшнl= 0;те фенотипни изследваниn= 3; потвърждавk= 2;т разнообразl= 0;ето на 17-те нови изолата Bacillus cereus/thu= ringiensis = и показват, че новият изолат от групата Bacillus subtilis е щам на Bacillus amyloliquefaciens. Представен = 77; един прост фенотипно дискриминаm= 0;ивен ключ, който може да се приложи за р= 072;зграничава&= #1085;е между тясно родствени ч = 83;енове на групата Bacillus cere= us/thuringiensis.

 

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