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Polyamine Profiles Within Genera of the Class Actinobacteria with U-Diaminopimelic Acid in the Peptidoglycan

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Polyamine Profiles Within Genera of the Class Actinobacteria with U-Diaminopimelic Acid in the Peptidoglycan International Journal of Systematic Bacteriology (1 999), 49, 179-1 84 Printed in Great Britain Polyamine profiles within genera of the class NOTE Actinobacteria with u-diaminopimelic acid in the peptidoglycan Hans-Jurgen Busse't and Peter Schumann2 Author for correspondence: Hans-Jurgen Busse. Tel: +43 1 25077 2128. Fax: +43 1 25077 2190. e-mail : Hans-Juergen. Busse @vu-wien.ac.at 1 Institute of Microbiology Polyamine patterns of coryne- and nocardioform representatives of the class and Genetics, University of Actinobacteria with u-diaminopimelic acid in the peptidoglycan, comprising Vienna, A-1030 Vienna, Austria strains of the genera A eromicrobium, Nocardioides, In trasporangium, Terrabacter, Terracoccus, Propioniferax, Friedmanniella, Microlunatus, * DSMZ-German Collection of Microorganisms and Luteococcus and Sporichthya, were analysed. The different polyamine patterns Cell Cultures GmbH, were in good agreement with the phylogenetic heterogeneity within this D-07745 Jena, Germany group of actinomycetes. Strains of the closely related genera Nocardioides and Aeromicrobium were characterized by the presence of cadaverine. The second cluster, consisting of the type strains of the species Friedmanniella antarctica, Propioniferax innocua, Microlunatus phosphovorus and Luteococcus japonicus, displayed as a common feature the presence of the two predominant compounds spermidine and spermine. The presence of putrescine was common to the type strains of the species Intrasporangium calvum, Terrabacter tumescens and Terracoccus luteus. Sporichthyapolymotpha, which is a representative of a separate line of descent, displayed spermidine as the predominant polyamine. These data indicate that polyamine patterns are suitable for the classification of actinomycetes with LL-diaminopimelic acid in the peptidoglycan. Keywords : polyamine patterns, chemotaxonomic classification, LL-diaminopimelic- acid-containing Actinobacteria Coryneform and nocardioform actinomycetes with LL- distinctly separated from the three clusters of diaminopimelic acid (LL-A,~~)as diagnostic diamino coryneform and nocardioform actinomycetes, which acid of their peptidoglycan are a biotechnologically comprise the following genera : (i) Nocardioides and interesting group of metabolically versatile bacteria. Aeromicrobium (Collins et al., 1994; Collins & Representatives of this group have, for example, the Stackebrandt, 1989; Miller et al., 1991 ; O'Donnell et capacity to accumulate polyphosphate (Nakamura et al., 1982; Tamura & Yokota, 1994) (Nocardioidaceae); al., 1995), to produce the antibiotic erythromycin (ii) Terrabacter (Collins et al., 1989), Terracoccus (Miller et al., 1991) and to transform steroids (Prauser et al., 1997) and Intrasporangium (Hayakawa & Kurokawa, 1963; Nobile et al., 1955). (Kalakoutskii, 1989) (Intrasporangiaceae); (iii) Organisms with LL-A,~~occupy different phylogen- Propioniferax (Yokota et al., 1994), Luteococcus etic lineages which represent five families within the (Tamura et al., 1994), Microlunatus (Nakamura et al., class Actinobacteria, as revealed by 16s rRNA se- 1995) and Friedrnanniella (Schumann et al., 1997) quence analyses (Prauser et al., 1997; Stackebrandt et (Propionibacteriaceae). These genera are distinguished al., 1997). The sporoactinomycetes Streptomyces from each other by their chemotaxonomic charac- (Streptomycetaceae) (Stackebrandt et al., 199 1) and teristics. The genera Nocardioides, Aeromicrobium, Sporichthya (Sporichthyaceae)(Rainey et al., 1993) are Luteococcus and Propioniferax share the peptido- glycan type A3y (Schleifer & Kandler, 1972), with a *Present address: lnstitut fur Bakteriologie, Mykologie und Hygiene, single glycine residue as interpeptide bridge. The Veterinarmedizinische Universitat Wien, Veterinarplatz 1, A-I 210 Wien, genera Terrabacter, Terracoccus and Intrasporangium Austria. are characterized by the cross-linkage of the A3y-type Abbreviation : LL-A,pm, LL-diaminopimelicacid. peptidoglycan via a triglycine-interpeptide bridge and 00717 0 1999 IUMS 179 H.-J. Busse and P. Schumann by a glycine residue bound to the a-carboxyl group of Corynebacterium (Altenburger et al., 1997). When the D-glutamic acid at position 2 of the peptide subunit. Nocardiodes albus strains IMET 7807T and IMET The genera Microlunatus and Friedmanniella are dis- 78 15 were grown on a mineral medium (Lindenbein, tinguished by the rare peptidoglycan type A3y' 1952), cadaverine was detected as the predominant (Schleifer & Seidl, 1985), with glycine at position 1 of compound. The high concentration of putrescine in the peptide subunit. The genera Nocardioides, the majority of strains of the genus Nocardioides when Terrabacter and Terracoccus have MK-8(H4) as their grown in R medium, in addition to cadaverine, appears major isoprenoid quinone, the genus Intrasporangium to be useful for differentiation from the genus shows MK-8, whereas the menaquinone MK-9(H4) is Aeromicrobium. The two species Aeromicrobium common to all other coryne- and nocardioform actino- fastidiosum and Aerornicrobium erythreum are phylo- mycetes with LL-A,pm. Fatty acid- and polar lipid genetically associated with the genus Nocardioides patterns are useful tools for the further differentiation (Tamura & Yokota, 1994) and are included in the of this group of organisms (Schumann et al., 1997). family Nocardioidaceae (Stackebrandt et al., 1997). Recently, the suitability of polyamine patterns for The polyamine patterns of these two species were classification of coryneform actinobacteria has been similar to members of the genus Nocardioides in demonstrated (Altenburger et al., 1997 ; Hamana, containing significant concentrations of cadaverine, 1995, 1996). However, these studies did not include which distinguished A erom icrob iumfas t idiosum I M ET representatives of the class Actinobacteria with LL- 7849T and Aeromicrobium erythreum NRRL B-338 lT A,pm or the data are difficult to interpret due to from the other LL-A,pm-containing actinobacteria. nonstandardized growth conditions. Thus, we However, the two species did not display identical analysed the polyamine composition of coryne- and polyamine patterns. Aerornicrobium fastidiosum IMET nocardioform actinomycetes with LL-A,pm to estimate 7849T contained a rather low concentration of poly- the value of this approach for classification of members amines and spermine was found to be the predominant of this phylogenetically heterogeneous group compound, whereas Aeromicrobium erythreum NRRL (Schumann et al., 1997). B-3381T was characterized by the second major com- pound, spermidine. Strains analysed are listed in Table 1. Biomass for polyamine analyses was obtained by submerged cul- The second polyamine similarity cluster consisted of tivation of the strains in R medium (Yamada & the phylogenetically closely related species Propioni- Komagata, 1972) or polyamine-free glucose/ ferax innocua, Microlunatus phosphovorus and Luteo- asparagine medium (MM) (Lindenbein, 1952) at 28 "C coccus japonicus, which are included in the family using a horizontal shaker run at 220 r.p.m. Cells were Propionibacteriaceae, and Friedmanniella antarctica harvested in the exponential phase of growth when (Schumann et al., 1997). Due to its phylogenetic 70% of the maximal optical density at 578 nm was position and similar chemotaxonomic characteristics reached. Because of the tendency to aggregation of Friedmanniella antarctica also belongs to the family Luteococcus japonicus IF0 12422T and Propioniferax Propionibacteriaceae (Schumann et al., 1997 ; innocua NCTC 11082T, their cultivation times were Stackebrandt et al., 1997). The type strains of these estimated. Sporichthya polymorpha IMET 7840T and four species, NCTC 11082T,JCM 9379T, IF0 12422T Friedmanniella antarctica AA-1042T did not grow in and AA- 1042*, respectively, contained polyamine submerged cultures, therefore cells were harvested patterns in which spermidine and spermine were the from R agar slant cultures. Polyamine extractions and predominant polyamines. Recently, six species of the analyses were performed as described recently genus Propionibacterium, including the LL-A,pm-con- (Altenburger et al., 1997). taining species Propionibacterium acidipropionici, Propionibacterium acnes, Propionibacterium jensenii, The analysis of the polyamine patterns of coryne- and Propionibacterium lymphophilurn, Propionibacterium nocardioform actinobacteria with LL-A,pm revealed propionicum Propionibacterium thoenii, the presence of at least four different profiles (Table 1). and have been The majority of strains, which belong to the genus shown to contain similar polyamine patterns Nocardioides, were characterized by the presence of (Hamana, 1995). All these six species contained high concentrations of the diamines putrescine and spermidine and spermine as the predominant com- cadaverine. The similarity in the polyamine patterns is pound in the polyamine pattern, demonstrating the close phylogenetic relatedness to the genera in agreement with the phylogenetic homogeneity of the Propioniferax, Luteococcus, Friedmanniella species of the genus Nocardioides (Collins et al., 1994). and Nocardiodes simplex Nocardiodes Microlunatus (Nakamura et al., 1995; Schumann et IMET 10283 and al., et al., et al., plantarum NCIMB 12834Twere found to contain rela- 1997; Tamura 1994; Yokota 1994). Based on the data shown, as well as already published tively low polyamine concentrations and displayed Propionibacterium, only cadaverine as the predominant diamine. The data on species of the
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