FEMS Microbiology Letters 100 (1992) 461-468 © 1992 Federation of European Microbiological Societies 0378-1097/92/$05.00 Published by Elsevier

461

FEMSLE 80008

Diversity of Pseudomonas plasmids: To what extent? A l e x a n d e r M. Boroni n Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Russia Received 11 June 1992 Accepted 27 June 1992

Key words: Pseudomonas; Plasmid; Incompatibility group

1. SUMMARY Results obtained in studies of the biology of

Pseudomonas plasmids are presented here as a mini-review. These data indicate that plasmids are ubiquitous in Pseudomonas, but the frequency of their occurren.ce varies greatly in particular species, or groups of species and in different microbial habitats. Some species of Pseudomonas, for instance P. aeruginosa, possess great diversity of plasmids both from the viewpoint of their incompatibility properties and their ability to endow bacteria with additional features such as resistance to antibiotics or heavy metals, degradation of xenobiotics or inhibition of phage development.

2. INTRODUCTION Plasmids control various properties of bacterial cells, including such practically important lea-

Correspondence to: A.M. Boronin, Laboratory of Biology of Plasmids, Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region, 142292, Russia.

tures as antibiotic resistance and ability to degrade toxic pollutants. Plasmids promote the horizontal transfer of genetic information between bacteria belonging to different taxonomic groups and play an important role in the evolution of bacteria [1]. Owing to the rapid progress of plasmid research, a specialized field of research concerned with the the biology of plasmids has evolved. This field covers the occurrence of plasmids in various bacteria and their contribution to the phenotype of the bacterial hosts, classification, natural history and possible uses. There is even a tendency to consider plasmids as, in a sense, organisms [2]. The genus Pseudomonas comprises a vast and rather diverse group of bacteria [3]. The fluorescent pseudomonads which include, among others, the species Pseudomonas aeruginosa, P. fluorescens, P. putida and P. syringae can be found in a variety of natural environments. It is hoped that research into plasmids of the fluorescent pseudomonads, which occupy a diversity of ecological niches, will contribute significantly to the development of the biology of plasmids as a whole. The following relevant points can be considered: (1) the extent of the occurrence of plasmids in fluorescent pseudomonads inhabiting specific

462 n a t u r a l e n v i r o n m e n t s ; (2) the p h e n o t y p i c f e a t u r e s d e t e r m i n e d by these plasmids; (3) the diversity of the p l a s m i d s d e t e r m i n i n g similar a n d d i f f e r e n t f e a t u r e s of b a c t e r i a ; a n d (4) the diversity o f the p l a s m i d s that occur in the b a c t e r i a l p o p u l a t i o n s of p a r t i c u l a r species.

3. R P L A S M I D S O F P. AERUGINOSA Two d e c a d e s of r e s e a r c h into P. aeruginosa R p l a s m i d s have illustrated the wide o c c u r r e n c e of antibiotic resistance p l a s m i d s in b a c t e r i a obt a i n e d from surgical p a t i e n t s a n d those with urinary tract infections a n d severe burns. T h e R p l a s m i d s of P. aeruginosa have b e e n classified into 13 i n c o m p a t i b i l i t y g r o u p s [4]. M o s t of the 260 P. aeruginosa R p l a s m i d s t h a t we have investigated ( T a b l e 1) could be classified into one o f t h e s e 13 i n c o m p a t i b i l i t y groups. A b o u t onethird of the p l a s m i d s b e l o n g to the IncP2 g r o u p [5] which is c h a r a c t e r i z e d by a large D N A size. W e m a d e an a t t e m p t to d e t e c t new R p l a s m i d s with small-size D N A with the aim of using t h e m s u b s e q u e n t l y as cloning vectors. H o w e v e r , all the small p l a s m i d s that we i s o l a t e d b e l o n g e d to the IncP4 g r o u p [6], a l t h o u g h s o m e p l a s m i d s d i f f e r e d from RSF1010, which can be c o n s i d e r e d a p r o t o type of p l a s m i d s in this i n c o m p a t i b i l i t y group. In a search for new p s e u d o m o n a d R plasmids, we investigated Pseudomonas strains i s o l a t e d from the w a s t e w a t e r s of a n t i b i o t i c - m a n u f a c t u r ing plants. O f 132 Pseudomonas strains, 114 w e r e P. aeruginosa isolates which c a r r i e d 19 p l a s m i d s b e l o n g i n g to i n c o m p a t i b i l i t y g r o u p s P1, P2, P3, P4 and P5. Two plasmids, pBS221 (Tc) (IncP1) [7] a n d pBS227 (Cb K m Tc Te) (IncP2) [8] w e r e f o u n d in strains of P. denitrificans a n d P. desmoliticum respectively. Several p l a s m i d s did not b e l o n g to any o f the k n o w n i n c o m p a t i b i l i t y groups. T h e b r o a d - h o s t r a n g e p l a s m i d pBS222 was assigned to a new i n c o m p a t i b i l i t y group, P14. A n o t h e r b r o a d - h o s t r a n g e p l a s m i d pBS52 differs from all known plasmids in its i n c o m p a t i b i l i t y p r o p e r t i e s . H o w e v e r , d e t a i l e d studies have shown it to b e the r e p l i c o n of p l a s m i d R S F 1 0 1 0 fused with p a r t of the replicon o f a n o t h e r p l a s m i d carrying tra g e n e s [9].

Table 1 R plasmids of P. aeruginosa Inc group

Plasmid a Properties b

P1 c P2 P3 c P4 c P5 P6 ~ P7 P9 PI0 Pll

pBS223 pBS12 pBS73 pBS95 pBSII Rms149 pBS14 R2 pBSRI RI51

P12 P13

R716 pM625

P4/P? c pBS52 P14 c pBS222

Size (kb)

Tc Tra + 61 Sm Cm Hg Mer Te Uv Tra + ~ 400 Sm Cm Tc Km Hg Su Tra + 88 Sm Su Ap Tra13 Sm Su Hg Pmr Cr Tra + 200 Sm Gm Cb Su Tra + 49 Cm Tra + 140 Sm Su Cb Uv Tra + 68 Km Gm Su Tp Hg Pmr Tra + 65 Km Gm Sm Sp Su Cb Tp Tra -81 Sm Hg Tra + nd Sm Km Gm Su Cb Tp Bor Tra + nd Sm Su Cb Tra + 38 Tc Tra + 17.2

a The prefix BS indicates the plasmids and their derivatives isolated at the Laboratory of Biology of Plasmids, Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences. pBS plasmids are according to refs. 5,6; other plasmids are as given in ref. 4. b Abbreviations: Ap, ampicillin; Bor, borate; Cb, carbenicillin; Cm, chloramphenicol; Cr, potassium bichromate; Gin, gentamicin; Hg, mercuric chloride; Km, kanamycin; Pmr, phenylmercuric acetate; Sm, streptomycin; Sp, spectinomycin; Su, sulfonamide; Tc, tetracycline; Te, potassium tellurite; Tp, trimethoprim; Uv, UV irradiation. Tra , transfer deficient. " Inc group harboring broad-host-range plasmids. nd = not determined.

Thus, most R p l a s m i d s of P. aeruginosa belong mainly to the i n c o m p a t i b i l i t y g r o u p s P1 t h r o u g h P5. S o m e R p l a s m i d s of P. aeruginosa could possibly be the p r o d u c t s of r e p l i c o n interactions o f t h e s e a n d o t h e r p l a s m i d s carrying various c o m b i n a t i o n s o f the same rep (inc) genes,

4. D E G R A D A T I V E

PLASMIDS

M a n y d e g r a d a t i v e ( D ) p l a s m i d s a r e known to c o n t r o l d e g r a d a t i o n of various o r g a n i c comp o u n d s including xenobiotics [10,11]. A n u m b e r of D p l a s m i d s that c o n t r o l the d e g r a d a t i o n of p a r t i c u l a r c o m p o u n d s , such as E - c a p r o l a c t a m [12,13], or n a p h t h a l e n e a n d salicylate [14-17] have

463

been isolated. Specifically, of 190 E-caprolactamdegrading strains isolated from various sources, 70 strains belonged to the genus Pseudomonas. About 90% of them bear CAP plasmids which determine degradation of ocaprolactam [12,18]. In 16 out of 30 strains of Pseudomonas spp. growing on naphthalene, we found conjugative plasmids (NAH) controlling the oxidation of this compound [16,17]. A more detailed investigation of CAP and NAH plasmids revealed great diversity in molecular size, conjugal transfer, resistance to heavy metal ions and assignment to particular incompatibility groups (Tables 2-4). However, all of these plasmids belong to a limited number of incompatibility groups (P2, P9 and P7); the NAH plasmids belong to incompatibility groups P7 and P9 (Table 4). In addition to being incompatible with plasmids of the IncP7 group, some NAH plasmids exhibit partial incompatibility with the IncP2 plasmids [17]. A similar phenomenon is observed with some IncP9 group CAP plasmids which are incompatible with IncP7 plasmids [21]. The NAH plasmids are transferred to P. aeruginosa PAO (usually used in the incompatibility studies of R plasmids) at a very low frequency, and thereafter many of them become non-conjugative. To classify D plasmids by their incompatibility properties, we used P. putida BSA [22]. Studies of P. aeruginosa R plasmid incompatibility properties in this system yield results identical to those obtained for the P. aeruginosa PAO system [22]. The naphthalene catabolic systems are thermosensitive and do not function in P. aeruginosa PAO at temperatures above 37-38°C. At 40-41°C, we observed a sharp increase in the instability of NAH plasmids, as well as formation of abnormal elongated partially lysed cells of P. aeruginosa PAO [29]. The data presented above suggest that most degradative plasmids belong to incompatibility groups P9 and P7, because the plasmids of these incompatibility groups have evolved and naturally occur in the fluorescent pseudomonads of the species P. putida, P. fluorescens and the like. This would explain the incapability of the genetic systems of the plasmids, controlling naphthalene degradation, to functionally express and stably

Table 2 CAP plasmids Plasmid

Molecular size (MDa)

Incompatibility group

Resistance to heavy metals ~

pBS262 pBS266 pBS271 pBS265 pBS267 pBS268 pBS270 pBS276

~ 300 ~ 300 ~ 300 100 100 70 70 50

P9 P2 P2 P9 P9 P9 P7, P9 P7, P9

Hg Te, Sn Te, Hg, Cr Hg Hg, Sn Hg, Sn Hg, Sn -

a Hg, mercuric chloride; Te, potassium tellurite; Sn, organotin compounds; Cr, potassium bichromate.

maintain the Nah phenotype at temperatures not characteristic of the mesophilic P. putida and P. fluorescens.

5. MEGA-SIZE PLASMIDS Of special interest are the large plasmids, belonging to the IncP2 group (Table 5). Some of them carry genes for antibiotic resistance; others, degradative genes. As a rule, they also bear genes for heavy metal resistance. A characteristic feature of these plasmids is that most of them code for resistance to tellurite. Several plasmids were found to carry the genes controlling resistance to organotin compounds [30].

Table 3 N A H plasmids Plasmid

Transfer frequency

pBS3 pBS219 pBS244 pBS2 pBS216 NPL-1 pBS

10 4 10 -4 I0 4 10 -4 10 3 10 3

a Silent genes of the

Molecular size (MDa) 110 130 100 100 60 58 115

rneta

Incompattibility group

Pathway of cathechol oxidation

P7 P7 (P2) P9 P7 P9 P9 P7

meta

pathway.

meta meta meta

a

meta

a

absent Naphthalene oxidation via gentisic acid

464 Table 4 Incompatibility groups of degradative plasmids Incompatibility group

Plasmid

Substrate

Reference

CAM

Camphor

[19]

P2

OCT pBS263, pBS264 pBS266, pBS271

Octane E-Caprolactam, e-Aminocapronic acid

[20] [21]

P7

pBS2, pBS3, pBS211, pBS213, pBS214, pBS217, pBS243 pBS4 TOL SAL pND50 NAH

Naphthalene Naphthalene

[22] [17]

Naphthalene Naphthalene Xylene, toluene Salicylate p-Cresol Naphthalene

[15] [23] [24] [25] [23]

P9

pND140, pND160 pWW60 NPL-41 pBS212, pBS216 pBS240, pBS244, pBS248 pBS262, pBS265, pBS267, pBS268, pBS269 pBS1004

Naphthalene Naphthalene Naphthalene Naphthalene Naphthalene

[26] [27] [22] [17]

e-Caprolactam, e-Aminocapronic acid

[21 ]

p-Toluenesulfonic acid

[28]

P7 (P2)

pBS218, pBS219

Naphthalene

[17]

P9 (P2)

pBS270, pBS276

E-Caprolactam, e-Aminocapronic acid

[21]

P l a s m i d s o f v a r i o u s i n c o m p a t i b i l i t y g r o u p s inhibit t h e g r o w t h o f P. aeruginosa a n d P. putida bacteriophage. Phage whose growth was inhibited

o n s t r a i n s c a r r y i n g p l a s m i d s o f t h e P5, P6, P9 a n d P10 i n c o m p a t i b i l i t y g r o u p s w e r e f o u n d . H o w e v e r , m o s t o f t e n , g r o w t h o f t h e p h a g e was s h o w n to b e

Table 5 Pseudomonas plasmids of P2 incompatibility group Bacteria

Plasmid

Incompatibility group

Properties a

P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa Pseudomonas sp. P. fluorescens Pseudomonas sp. Pseudomonas sp.

pBS79 pBS10 pBS33 pBS31 pBS218 pBS219 pBS266 pBS271

P2 P2 P2 P2 P7 (P2) b P7 (P2) b P2 P2

Sm Km Tc Gm Hg Te Tra + Sm Su Hg Te Sn Tra + Sm Hg Cr Te Uv Tra + Sm Tc Cm Su Hg Te Tra + Nab Sal Te Tra + Nab Sal Te Tra + Cap Te Sn Tra + Cap Te Hg Cr Tra +

a Abbreviations not given in footnotes to Tables 1 and 2: Cap, ability to degrade e-caprolactam; Nah, ability to degrade naphthalene; Sal, ability to degrade salicylate. Plasmids pBS218 and pBS219 exhibit a partial incompatibility with IncP2 plasmids.

465 inhibited by the presence of plasmids belonging to the IncP2 group [12,31]. Plasmids in this group differed in the spectrum of bacteriophages whose growth they inhibited. The IncP2 CAP plasmid pBS271 (Table 5) is unique because it suppresses the growth of a broad range of P. aeruginosa and P. putida phage. The maintenance of the plasmid and the expression of the plasmid genes is the energy price that the bacteria must pay for harboring the plasmids. This price, to a certain extent, increases with the size of the plasmid. Indeed, this tendency was revealed in the growth rate studies of Escherichia coli strains carrying various R plasmids [32]. Interestingly, despite their enormous sizes, the IncP2 plasmids that we investigated are very stable under various growth conditions. These data suggest that these plasmids have evolved mechanisms that ensure their stable maintenance in the bacterial population despite the metabolic burden imposed upon their host cell.

6. PLASMIDS OF P. SYRINGAE AND RHIZOSPHERE PSEUDOMONAS One of the most widespread phytopathogenic bacterial species is P. syringae, which is classified into 41 pathovars. We studied the distribution of plasmids in 49 P. syringae strains of 17 pathovars. The plasmids range in size from 3 to 135 kb. In the P. syringae strains studied here and also by other investigators [33,34] no plasmids of over 150 kb were found. Apparently, large plasmids characteristic of the IncP2 group of Pseudomonas have not been found in P. syringae strains. In six strains of the pathovars holci, astrofaciens, pisi, lachrymans, phaseolicola and glycinea, three or four plasmids were found. The functions of the plasmids that we investigated, as well as those of most of the other P. syringae plasmids, are not known. In rhizosphere pseudomonads, including plant growth-promoting rhizobacteria, we found only a minor amount of cryptic plasmids with molecular sizes of 60 to 100 MDa. Some plasmids are incompatible with IncP7 plasmids.

7. CONCLUSIONS Plasmids are ubiquitous in Pseudomonas. On the other hand, the frequency of occurrence of plasmids greatly varies in particular species or groups of species of these bacteria. Virtually all strains of P. syringae studied contained plasmid DNA. The frequency of occurrence also depends on the ecological niche from which the bacteria were isolated. For instance, the frequency of occurrence of R plasmids in P. aeruginosa was significantly higher in hospital strains than in the bacteria isolated from water or soil. The same is true for the appearance of D plasmids in the strains of the P. putida-P, fluorescens group: their frequency of occurrence was far greater in bacteria isolated from habitats polluted with xenobiotics than in those isolated from the plant rhizosphere. The plasmids found in various Pseudomonas species reveal a diversity in their incompatibility groups that characterize them as replicons. Strains of P. aeruginosa contain a greater diversity of plasmids than the P. putida-P, fluorescens strains. On the basis of their incompatibility, all the D plasmids of the P. putida-P, fluorescens group can be classified into three groups: IncP2, IncP7 and IncP9. Although plasmids are prevalent in Pseudomonas and differ in many characteristics, it can be predicted that the number of replicons carrying antibiotic resistance or degradative genes is likely to be limited, especially in any one particular species or group of species. Many of these replicons have already been discussed. New types of replicons will, most probably, be broad-hostrange plasmids or fused replicons. Thus, natural bacterial populations of Pseudomonas consist of plasmids which determine the same or similar phenotypes differing in some features. Our preliminary data support the suggestion that in nature the D plasmid-host combinations give rise to greater diversity of bacterial strains capable of degrading particular xenobiotics than generally thought. In part this is due to the fact that a genetic system which controls, for instance, the degradation of naphthalene and salicylate also allows some catabolism of their

466

numerous chloro- or methyl derivatives [27,35,36]. That is why the bacteria have to modify this genetic system to adjust it to the environmental conditions by turning on or off particular genes or blocks of genes [37-42]. Studies of this type of microbial diversity are closely associated with the problem of the release of genetically modified microorganisms into the natural environment. Attention should be paid not only to the fate of the genetically modified microorganisms in the environment, but also to the diversity of the indigenous microbial community which already contains various naturally occurring D plasmids. We should be aware that these plasmids are also the products of genetic engineering performed in vivo by the microorganisms themselves.

ACKNOWLEDGEMENTS I am grateful to the staff of the Laboratory of Plasmid Biology; our collaborative work formed the basis for this mini-review. I also thank V.D. Selivanov for technical assistance. This study was supported by the Russian Academy of Sciences.

REFERENCES [1] Reanney, D. (1976) Bacteriol. Rev. 40, 552-590. [2] Datta, N. (1985) In: Plasmids in Bacteria (Helinski, D.R., Cohen, J.N., Crewell, D.B., Jackson, D.A. and Hollander, H., Eds.), pp. 3-16, Plenum Press, New York. [3] Palleroni, N.J. (1986) In: The Bacteria, vol. X, (Sokatch, J.R., Ed.), pp. 3-26. Academic Press, Orlando, FL. [4] Jacoby, G.A. (1986) In: The Bacteria, Vol. X. The biology of Pseudomonas (Sokatch, J.R., Ed.), pp. 265-292. Academic Press, Orlando, FL. [5] Anisimova, L.A. and Boronin, A.M. (1981) Antibiotiki 6, 450-456 (in Russian). [6] Boronin, A.M., Anisimova, L.A., Kozlova, E.V. and Erova, T.E. (1985) In: Transferable Antibiotic Resistance (Mitsuhashi, S., Krf:m(~ry, V., Antal, M. and Rosival, L., Eds.), pp. 353-355. Avicenum, Prague, Czechoslovakia. [7] Parfenova, O.V., Anisimova, L.A. and Boronin, A.M. (1990) Genetika 6, 981-989 (in Russian). [8] Kozlova, E.V. and Boronin, A.M. (1983) Antibiotiki 10, 729-733 (in Russian). [9] Polevoda, B.V., Tsoi, T.V. and Boronin, A.M. (1987) Genetika 10, 1823-1831 (in Russian).

[10] Frantz, B. and Chakrabarty, A.M. (1986) In: The Bacteria, Vol. X, (Sokatch, J.R., Ed.), pp. 295-323. Academic Press, Orlando, FL. [11] Sayler, G.S., Hooper, S.W., Layton, A.C. and King, H.J.M. (1990) Microb. Ecol., 19, 1-20. [12] Boronin, A.M., Grishchenkov, V.G., Kulakov, L.A. and Naumova, R.P. (1986) Mikrobiologiya 55, 231-236 (in Russian). [13] Boronin, A.M., Naumova, R.P., Grishchenkov, V.G. and Iljinskaya, O.N. (1984) FEMS Microbiol. Lett. 22, 167170. [14] Boronin, A.M., Borisoglebskaya, A.N. and Starovoytov, I.I. (1977) Dokl. AN SSSR 235, 494-496 (in Russian). [15] Skryabin, G.K., Kochetkov, V.V., Eryomin, A.A., Perebityuk, A.N., Starovoytov 1.1. and Boronin, A.M. (1980) Dokl. AN SSSR 250, 212-215 (in Russian). [16] Kochetkov, V.V. and Boronin, A.M. (1984) Mikrobiologiya 53, 639-645 (in Russian). [17] Kochetkov, V.V. and Boronin, A.M. (1985) Genetika 21, 522-529 (in Russian). [18] Esikova, T.Z., Grishchenkov, V.G. and Boronin, A.M. (1990a) Mikrobiologiya 4, 547-552 (in Russian). [19] Jacoby, G.A. (1975) In: Microbiology-1974 (Schlessinger, D., Ed.), pp. 36-42. American Society of Microbiology, Washington, DC. [20] Jacoby, G.A. (1977) In: Microbiology-1977 (Schlessinger, D., Ed.), pp. 119-126. American Society of Microbiology, Washington, DC. [21] Esikova, T.Z., Grishchenkov, V.G., Kulakov, L.A., Morenkova, M.A. and Boronin, A.M. (1990) Mol. Genet. Mikrobiol. Virusol. 4, 25-28 (in Russian). [22] Boronin, A.M., Kochetkov, V.V. and Skryabin, G.K. (1980) FEMS Microbiol. Lett. 7, 249-252. [23] White, C.P. and Dunn, H.W. (1978) Genet. Res. 32, 207-213. [24] Korfhagen, T.R., Sutton, L. and Jacoby, G.A. (1978) In: Microbiology-1978 (Schlessinger, D., Ed.), pp. 221-224. American Society of Microbiology, Washington, DC. [25] Hewetson, L., Dunn, H.M. and Dunn, N.W. (1978) Genet. Res. 32, 240-255. [26] Dunn, N.W., Dunn, H.M. and Austen, R.A. (1980) J. Gen. Microbiol. 117, 329-333. [27] Cane, P.A. and Williams, P.A. (1982) J. Gen. Microbiol. 128, 2281-2290. [28] Dubeikovsky, A.N., Taranova, L.A., Naumov, A.V., Gafarov, A.B. and Boronin, A.M. (1992) Mikrobiologiya (in press) (in Russian). [29] Kochetkov, V.V. and Boronin, A.M. (1983) Mikrobiologiya 52, 27-32 (in Russian). [30] Anisimova, L.A., Andreeva, A.L and Boronin, A.M. (1985) Antibiotiki i Med. Biotechnologiya 5, 337-341 (in Russian). [31] Kulakov, L.A., Mazepa, V.N. and Boronin, A.M. (1984) Mikrobiologiya 53,471-475 (in Russian). [32] Ziind, P. and Lebek, G. (1980) Plasmid 3, 65. [33] Panopoulos, N.J. and Peet, R.C. (1985) Annu. Rev. Phytopathol. 23, 381-405.

467 [34] Piwowarski, J.M. and Shaw, P.D. (1982) Plasmid 7, 85-92. [35] Kulakova, A.N. and Boronin, A.M. (1989) Mikrobiologiya 58, 236-241 (in Russian). [36] Timmis, K., Lehrbach, P.R., Harayama, S., Dou, R.H., Mermod, N., Bas, S., Leppik, R., Weightman, A.T., Reineke, W., Knackmuss, H.-J. (1985) In: Plasmids in Bacteria, (Helinski, D., Cohen, C.N., Clewel, D.B., Jackson, D.A., Hollander, A., Eds.), pp. 719-739. Plenum Press, New York. [37] Boronin, A.M., Starovoytov, I.I., Borisoglebskaya, A.N., and Skryabin, G.K. (1976) Dokl. AN SSSR 228, 962-965 (in Russian). [38] Kosheleva, I.A., Tsoi, T.V., Kulakova, A.N. and Boronin, A.M. (1986) Genetika 10, 2389-2397 (in Russian).

[39] Tsoi, T.V., Kosheleva, I.A. and Boronin, A.M. (1986) Genetika 11, 2702-2712 (in Russian). [40] Boronin, A.M. and Tsoi, T.V. (1989) Genetika 4, 581-594 (in Russian). [41] Tsoi, T.V., Kosheleva, I.A., Nagayeva, M.V., Bezborodnikov, S.O., Gribanova, L.G., Kulakova, A.N. and Boronin, A.M. (1990) In: Abstract Book of 6th International Symposium on Genetics of Industrial Microorganisms (GIM 90), Strasbourg, p. 192. [42] Boronin, A.M., Kulakova, A.N., Tsoi, T.V. Kosheleva, I.A. and Kochetkov, V.V. (1988) Dokl. AN SSSR 229, 237-240 (in Russian).

Diversity of Pseudomonas plasmids: to what extent?

Results obtained in studies of the biology of Pseudomonas plasmids are presented here as a mini-review. These data indicate that plasmids are ubiquito...
444KB Sizes 0 Downloads 0 Views