Stepwise increase of elongation rate in individual hyphae of <i>Streptomyces granaticolor</i> during outgrowth

Kretschmer, Sigrid

doi:10.1002/jobm.3620280106

Cited by 11 publications

(9 citation statements)

References 29 publications

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“…Thus, it has been reported that germ tubes of S. hygroscopicus elongated exponentially [3], whereas in S. coelicolor they elongated linearly [5]. Exponential kinetics of elongation were initially also reported for S. granaticolor [4], but further studies using a more detailed mode of observation revealed that in this microorganism the germ tubes elongate linearly [11]. All these observations have been made on cultures of streptomycetes grown on solid media.…”

Section: Discussionmentioning

confidence: 96%

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Synchronous germination of Streptomyces antibioticus spores: Tool for the analysis of hyphal growth in liquid cultures

Miguélez

Martín

Hardisson

et al. 1993

FEMS Microbiology Letters

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We have devised a method for obtaining synchronous and dispersed growth of Streptomyces antibioticus in liquid cultures. After ultrasonic treatment, most of the spores germinated at the same time, yielding hyphae very similar in length. Dispersed growth was achieved in media without Ca2+ and in which the levels of Fe2+ and Mg2+ were carefully controlled. Studies on the kinetics of growth carried out with synchronous cultures of young hyphae revealed a multiphasic pattern of hyphal elongation, with successive periods of linear growth and changes in growth rate at defined intervals.

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Section: Discussionmentioning

confidence: 96%

“…Using these cultures it was possible to investigate the pattern of growth during the initial steps of hy-phal development. This topic has been the subject of contradictory reports [11]. Thus, it has been reported that germ tubes of S. hygroscopicus elongated exponentially [3], whereas in S. coelicolor they elongated linearly [5].…”

Section: Discussionmentioning

confidence: 99%

Synchronous germination of Streptomyces antibioticus spores: Tool for the analysis of hyphal growth in liquid cultures

Miguélez

Martín

Hardisson

et al. 1993

FEMS Microbiology Letters

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“…Looking for a factor which may be responsible for the timing of septation, a coordination by means of DNA replication events seems, at first sight, to be missing. Namely, even at very slow rates of growth (doubling times of several hours) the new-born daughter cells contain 6 (in c2) and 8 (in c l ) nucleoids, since the unit cell length in vitro accounts for 1.1 pm (KRETSCHMER and KUMMER 1987). But, when for the fast growing cultures the time T between two successive septations is calculated (Table 2), the values are quite identical to the replication time C, which was 46 min in glucose-peptone medium (KRETSCHMER 1988), and 52 min in glucose-casamino acids medium (z = 96 min, KUMMER and KRETSCHMER 1986).…”

Section: Discussionmentioning

confidence: 99%

“…Namely, even at very slow rates of growth (doubling times of several hours) the new-born daughter cells contain 6 (in c2) and 8 (in c l ) nucleoids, since the unit cell length in vitro accounts for 1.1 pm (KRETSCHMER and KUMMER 1987). But, when for the fast growing cultures the time T between two successive septations is calculated (Table 2), the values are quite identical to the replication time C, which was 46 min in glucose-peptone medium (KRETSCHMER 1988), and 52 min in glucose-casamino acids medium (z = 96 min, KUMMER and KRETSCHMER 1986). This similarity between Tand Cat fast rates of growth leads us to the conclusion that the timing of septation is determined with the rhythm of DNA replication, if the apical cell has attained a certain length.…”

Section: Discussionmentioning

confidence: 99%

“…Lcl, = Lcl + --2 These two equations are based on the fact that older hyphae elongate continuously at a constant rate (KRETSCHMER 1988). specific growth rate of the cultures (h-') and doubling time of the cultures (min), determined photometrically average length of the hyphal growth unit, where L is the length of a mycelium and Nits number of hyphal tips (CAIDWELL and TRINCI 1973) calculated elongation rate of individual hyphae (pm h-') by using the equation a = p (L/N) (BERGTER 1978) In further calculations this average value of a was used, although the real a of cl is obviously a little above of the whole mycelium, since newborn hyphae (for about 1 h) elongate at a slower rate than older ones .…”

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Septation behaviour of the apical cell in Streptomyces granaticolor mycelia

Kretschmer¹

1989

J. Basic Microbiol.

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The septation behaviour of the apical hyphal cell, which solely brings about hyphal elongation, was studied using mycelia grown at different specific growth rates (p) (chemostat and batch cultures). After cell wall staining it was found that both the apical cell (cl) and the adjacent subapical cell (c2) were generally unbranched. Thus, their length (L) could be easily determined.As the growth rate decreased, Lcl as well as Lc2 decreased, but cells smaller than 5 pm were not observed, even at extremely slow rates of growth (p = 0.06 h-'). The largest cells were observed in rich media, where Lcl attained 41 pm. Since Lc2 represented the length of one of the new-born daughter cells of cl, the distribution curves of Lc2 were used to look for regularity of septation. Especially at slow rates of growth, the curves indicated that in cl septation did not occur randomly. By using Lc2 the interdivision time Tof cl wascalculated. At fast rates of growth it was identical to the earlier determined replication time C, indicating that in mature hyphae septation was coupled to the rounds of DNA replication.Lcl and Lc2 were used to calculate the length of cl at birth and at the start of septation. It was found that upon septation the appearing daughter cells were differently sized. Depending on the growth rate, the apically situated daughter cell was 1.37 to 1.81 times larger than the subapical daughter (c2). Based on the functional heterogeneity of the sister cells a hypothesis was invented, which could explain the asymmetric septation pattern. It involves the existence of a period S between the determination of the septum site at median position and the actual process of septum formation. The duration of S was calculated, and its correlation to the T and C values at the corresponding growth rates was discussed. Two mechanisms could be distinguished, which were responsible for the immense increase of Lcl at fast rates of growth.The hyphae of Streptomyces mycelia are septated by cross walls. Each hyphal length surrounded by a continuous envelope was regarded as a single cell (KRETSCHMER 1982). Since Streptomyces hyphae elongate solely at the hyphal tip ( SCHUHMANN und BERGTER 1976, LOCCI and SCHAAL 1980, BRANA et al. 1982 only the apically situated cell contributes to hyphal growth. The conversion of nongrowing subapical cells into growing ones by branch formation will not be regarded here.Until now, it was not known, whether the growing apical cell exhibits a regulated pattern of septation, or whether cross wall formation occurs rather randomly. Because the filamentous hyphal cells contain numerous nucleoids (KRETSCHMER and KUMMER 1987) a simple coordination between D N A replication and septation as is expressed in the single cell eubacteria (DONACHIE 1979, NANNINGA and WOLDRINGH 1985) seems to be missed.In order to describe the septation pattern of the apical cell in streptomycetes, the apical hyphal region of Streptomyces granaticolor was quantitatively analyzed at cellular level. For the timing as well as for the location o...

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Correlation between branching and elongation in germ tubes of Streptomyces granaticolor

Kretschmer¹

1991

J. Basic Microbiol.

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With four individual germ tubes (GTs), the distinct time of birth of branches was correlated to the kinetics of GT-elongation. During the first three hours, corresponding to five doubling times, branching was suppressed. The time of birth of the first branch (tbl) coincided with the 51h step of the typical stepwise increase of the GT elongation rate (GI). During this time, the quasi-exponential kinetics of a changed to linear kinetics, which was attained either at the 51h of 61h a-step. At the 51h step, the quotient of successive U-values had been reduced from 2 at the beginning of outgrowth to 1.2.Once the first branch had been formed, further branches appeared as clusters (additional 2, 4, and 8 branches) at D-intervals representing the doubling time of the hyphal length.The first branch appeard always in the vicinity of the spore. The average distance to the spore of 6.6 pm corresponded to four unit cells. At t b l , the unbranched region located between the first branch and the tip of the GTs was 42 pm long. The data concerning timing and location of the first branching in GTs suggest that initiation of branching was dependent on the accumulation of envelope precursors.Hitherto it has not been known how the formation of branches in mycelia of streptomycetes is regulated. Studies on the frequency of branching of mycelia grown in liquid media revealed that it was dependent on the growth rate, as well as on the composition of the media (RIESENBERG and BERGTER 1979, KRETSCHMER 1982). For example, in chemostats, with increasing growth rate the frequency of branching increased in the case of carbon limitation, but decreased, when nitrogen was limiting (KRETSCHMER 1985). This fact indicates that the formation of branches depends on the metabolism.However, this dependency may exist only indirectly. Morphogentic studies of the highly variable procaryotes Agrobacterium tumefactiens and Oerskovia xanthineolytica indicated that branches were initiated when the elongation rate (a) of the cell and hypha, respectively, approached its maximum value, while a, , , itself was dependent on the growth conditions (FUJIWARA andFUKUI 1974, KRETSCHMER 1981).In streptomycetes, the mode of increase of a in growing hyphae occurs stepwise until amax is attained (KRETSCHMER 1988). Using germ tubes of these organisms, the question of whether and how the mode of branching is correlated to the elongation behaviour can readily be studied.In the present paper, the timing and location of the first branching in germ tubes was correlated to their elengation behaviour by analyzing series of micrographs taken from individual germ tubes growing on agar medium. Materials and methodsThe organism used was Streptomyces granaticolor strain ETH 7437. Spores were harvested from 8 days old slant cultures grown on oat meal agar and washed twice with distilled water. Methods used for microcultivation and phase contrast microscopy were as described before (KRETSCHMER 1978). The medium used for microcultivation was glucose-pepton agar (KRETSCHMER 1982) enriched...

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Stepwise increase of elongation rate in individual hyphae of Streptomyces granaticolor during outgrowth

Cited by 11 publications

References 29 publications

Synchronous germination of Streptomyces antibioticus spores: Tool for the analysis of hyphal growth in liquid cultures

Synchronous germination of Streptomyces antibioticus spores: Tool for the analysis of hyphal growth in liquid cultures

Septation behaviour of the apical cell in Streptomyces granaticolor mycelia

Correlation between branching and elongation in germ tubes of Streptomyces granaticolor

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