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Early Stages of Conjugation in Escherichia Coli ROY CURTISS, III, LUCIEN G

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Early Stages of Conjugation in Escherichia Coli ROY CURTISS, III, LUCIEN G JOURNAL OF BACTERIOLOGY, Nov. 1969, p. 1091-1104 Vol. 100, No. 2 Copyright 0 1969 American Society for Microbiology Printed in U.S.A. Early Stages of Conjugation in Escherichia coli ROY CURTISS, III, LUCIEN G. CARO, DAVID P. ALLISON, AND DONALD R. STALLIONS Biology Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37830 Received for publication 8 September 1969 We initiated these studies to learn more about the initial events during bacterial conjugation and to optimize conditions for their occurrence. We found that cells in donor cultures grown anaerobically prior to mating have (i) a higher mean number of F pili per cell, (ii) longer F pili, (iii) a higher probability of forming specific pairs with F- cells, and (iv) a faster rate of initiation of chromosome transfer than cells grown aerobically. The growth medium for the donor culture also influences these same parameters: a rich medium is superior to a completely synthetic medium. Starvation of donor cells in buffered saline or for a required amino acid results in (i) a loss of F pili, (ii) a loss in the ability of donor-specific phages to adsorb, (iii) a loss of ability to form specific pairs with F- cells and to yield recombinants, and (iv) an increase in recipient ability. These changes occur as a function of starvation time, and at rates which are dependent on the conditions of prior growth and starvation of the donor culture. Either treatment provides a rapid method for the production of F- phenocopies from donor cultures. Resynthesis ofF pili by cells within a starved donor culture commences very soon after restoration of normal growth conditions, but full restoration of donor ability, as measured by recombinant yield, occurs at a slower rate. We found, along with other investigators, that F pili are essential for specific pair formation. We also found, however, that the presence of F pili is not sufficient for display of donor ability, nor is the absence of F pili enough for cells to exhibit recipient ability. This suggests, therefore, that one or more components, in addition to F pili, are necessary for the conversion of specific pairs to effective pairs (or for chromosome mobilization, or both) and for preventing donor cells from act- ing as recipients. On the basis of our results, we suggest optimal conditions for achieving high mating efficiencies. Bacterial conjugation in Escherichia coli K-12 under the control of the fertility factor F (2-4) is initiated by the formation of specific pairs be- constitute the F-specific antigen (20), and are tween donor and recipient cells. De Haan and obligatory for specific pair formation (2, 18, 28, Gross (12) experimentally defined a specific pair 29). Brinton's group (2-4, 28, 29) and others as a donor-recipient cell union that is stable dur- (18, 21, 32) have further suggested that F pili may ing gentle dilution of the mating cultures. The function as conjugation tubes in addition to their next step is the conversion of a specific pair to an role in specific pair formation. effective pair, and it must involve the establish- Our investigations on the early stages of bac- ment of a conjugation tube or bridge between terial conjugation were prompted by a desire to donor and recipient cells that would permit sub- test these ideas, to develop mating conditions for sequent transfer of donor genetic information. achieving maximal fertility of donor cultures, Mobilization of the donor chromosome (i.e., its and to provide explanations for the loss of donor preparation for linear sequential transfer) could ability caused by starvation (11, 14, 15, 22) and occur during specific and effective pair formation by prolonged growth (6). A lengthy discussion of or after effective pair formation. These three all the published data and ideas concerning the events must precede transfer of the donor chro- early stages of bacterial conjugation has been mosome during conjugation. After the discoveries published (10) and will not be repeated here. that donor cells possess a donor-specific antigen (30) and are able to adsorb donor-specific ribo- MATERIALS AND METHODS nucleic acid (RNA) phages (24, 25) to filamen- Media. The synthetic media used were minimal tous external structures (7) called F pili (4), it was liquid (ML) and minimal agar (MA) (8, 11), minimal demonstrated that these F pili are synthesized mating medium (8, 11), and M9 (1); these were supple- 1091 1092 CURTISS ET AL. J. BACTERIOL. mented with Casamino Acids (Difco), carbon sources, mating was no more than 2 X 108/ml. All conditions and other growth factor requirements at levels previ- were kept optimum for the recovery of the maximum ously listed (11). L broth and agar (23) and Penassay possible number of recombinants. The justification for Broth and Agar (Difco) were used as complex media. these procedures and the methods for interruption of Buffered saline with gelatin (8) was used for starvation mating and recombinant selection have been pre- of bacteria. sented (11). Bacteria. The bacterial strains used to obtain the Electron microscopy and enumeration of F pili data presented in this manuscript are listed in Table 1. length and number. The general procedures for attach- The procedures for maintaining bacterial strains, for ment of the donor-specific RNA and DNA phages to isolating and characterizing mutants, and for perform- donor cells and for preparation and examination of ing controls on stability of mating-type characteristics, specimens in the Siemens-Elmiskop I electron micro- on recombinant type purity, etc., have been described scope have been described (5). F pili were specifically (11). identified by their ability to attach any of the RNA Bacteriophages and antiserum. Ultraviolet-irradiated donor phages along their lengths (4, 7) and the DNA purified T4 and T6 (2.5 X 103 ergs/mm2) were used to phage fl to their tips (5). MS-2 was the phage rou- interrupt matings. Unadsorbed phages were neutral- tinely used for this purpose, sometimes in combina- ized by phage-specific antisera obtained after repeated tion with fl. Donor phages were added to samples of injections of rabbits with purified phage as described donor cultures in the presence of 2.5 X 10-2 M KCN by Adams (1). and, after 5 to 10 min at 37 C, OS04 was added to Donor-specific RNA phages R17 (supplied by R. 0.4% final concentration. A drop of the suspension K. Fujimura), M&2 (supplied by J. Schnell), f can (sup- was then immediately placed on each of two to four plied by C. Davem), MS-2 (supplied by A. J. Clark), specimen screens for each bacterial culture being and Q,B (supplied by S. Spiegelman), and the donor- tested. After 5 to 6 min to allow bacteria to attach to specific deoxyribonucleic acid (DNA) phage fl the screen, the remaining liquid was sponged off with (supplied by June Rothman Scott) were propagated filter paper and replaced by drops of 1% phospho- on a variety of donor strains by infection of cells from tungstic acid (PTA) in 0.1 M ammonium acetate a near stationary phase culture grown in L broth. (pH 5.5). The excess PTA was removed immediately CaCl2 was added to 2.5 X 10- M at the time of and the specimen screens were then allowed to dry in infection. Other techniques and procedures were air before examination in the electron microscope. as described by Adams (1). The number of F pili per cell were determined for Mating procedures. Donor strains were grown under 50 to 200 cells per preparation by examining different a variety of conditions. The recipient parents were al- fields of the specimen screens, whereas the lengths of F ways grown with vigorous aeration (11), and matings pili were measured on projected electron micrographs. were performed in 10-ml volumes in 125-ml micro- Corrections of mean numbers and lengths of F pili fernbach flasks (Beilco) immersed, to within 5 to 10 for obscuration of F pili by cells (27) were not made, mm of the metal caps, in a waterbath at 37 C. The since there was no way to objectively calculate the donor-recipient cell ratio was between 1 :10 and 1: 20, corrections to be used. In addition, the application of and the total bacterial cell density at the beginning of such corrections would only result in relative increases TABLE 1. Bacterial strainsa Strain Mating Relevant genotype" Derivation no. type x57 Hfr H T68 strs cycB thi O-thr ara leu proB* *met F 3000e x99 F- thr- lew- T6J str7 cyc' thi Xl2d X148 F- leu- T6r purE- trpj strr cyc' thi- x9C x313 Hfr P4X6 T68 X+ T48 thy- strs mer cyc8 O-proB proA leu ara * * lac F AB2383 x462 F- leu- proA- T6r purE- trp- lysF strr metE- cyc8 thi- X148 x493 Hfr ORll prototroph T68 T4' str8 cyc8 O-proB proA leu ara* lac F xl5c x503 Hfr OR21 prototroph T6J T4J str8 cyc8 0-proC T6 purE pyr * lac F xl5c x584 Hfr OR41 proB-lac- T68 thy- str cyc' O-thr ara leu proB... met F x354c X624 Hfr OR21 pyrA- TPr T6 T4r strt cycs x503 x679 Hfr CR34 leuc T68 str cyc' O-thr ara leu proB* met F 26 X820 F- thr- proC- T6r purE- pyr- his strt cycr x723c The nomenclature is essentially that of Demerec et al. (13), with the exceptions noted by Curtiss (9). All mutations conferring auxotrophic requirements are listed, but mutations conferring inability to utilize carbon sources have been omitted for brevity. All strains are nonlysogenic unless otherwise indi- cated. c See Curtiss et al.
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