FEMS Microbiology Reviews 25 (2001) 269^283 www.fems-microbiology.org Cell wall teichoic acids: structural diversity, species speci¢city in the genus Nocardiopsis, and chemotaxonomic perspective Irina B. Naumova a;*, Alexander S. Shashkov b, Elena M. Tul'skaya a, Galina M. Streshinskaya a, Yuliya I. Kozlova a, Nataliya V. Potekhina a, Lyudmila I. Evtushenko c, Erko Stackebrandt d a School of Biology, Lomonosov Moscow State University, Moscow 119899, Russia b Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, Leninsky prospect 47, Moscow 117913, Russia c VKM ^ All Russian Collection of Microorganisms, Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino 142292, Moscow Region, Russia d DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany Received 11 September 2000; received in revised form 10 November 2000; accepted 15 November 2000 Abstract Data on the structures of cell wall teichoic acids, the anionic carbohydrate-containing polymers, found in many Gram-positive bacteria have been summarized and the polymers of the actinomycete genus Nocardiopsis have been considered from the taxonomic standpoint. The structures of these polymers or their combinations have been demonstrated to be indicative of each of seven Nocardiopsis species and two subspecies, verified by the DNA^DNA relatedness data, and to correlate well with the grouping of the organisms based on 16S rDNA sequences. As each of the intrageneric taxa discussed is definable by the composition of teichoic acids, the polymers are considered to be valuable taxonomic markers for the Nocardiopsis species and subspecies. The 13C NMR spectra of the polymers, data on the products of their chemical degradation, and distinguishing constituents of whole cell walls derived from teichoic acids are discussed, which are useful for identification of certain polymers and members of the genus Nocardiopsis at the species and subspecies level in microbiological practice. ß 2001 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. Keywords: Teichoic acid; Taxonomy; Actinomycetes; Nocardiopsis Contents 1. Introduction .......................................................... 270 2. The genus Nocardiopsis .................................................. 271 3. Structural types of cell wall teichoic acids . .................................. 271 3.1. Poly(polyol phosphate) teichoic acids (type I) . ............................ 272 3.2. Poly(glycosylpolyol phosphate) teichoic acids (type II) . ....................... 273 3.3. Poly(polyol phosphate-glycosyl phosphate) teichoic acids (type III) . ............. 273 3.4. Poly(polyol phosphate-glycosylpolyol phosphate) teichoic acids, mixed structure (type IV).............................................................. 273 4. Determination of teichoic acid structures . .................................. 273 5. Cell wall teichoic acids of Nocardiopsis species and subspecies . .................. 273 5.1. N. dassonvillei subspecies . ............................................ 274 5.2. N. trehalosi ........................................................ 274 5.3. N. tropica ......................................................... 274 * Corresponding author. Fax: +7 (095) 939 43 09; E-mail: [email protected]; [email protected] Abbreviations: GalNAc, N-acetylgalactosamine; Glc, glucose; GlcNAc, N-acetylglucosamine; Gro, glycerol; GroP, glycerol monophosphate; GroP2, glycerol diphosphate; Pyr, pyruvic acid; Rib-olP, ribitol monophosphate; Rib-olP2, ribitol diphosphate; Rib-olP3, ribitol triphosphate; Succ, succinic acid; TA, teichoic acid; tr, trace; sn, stereospeci¢c numbering 0168-6445 / 01 / $20.00 ß 2001 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. PII: S0168-6445(00)00064-4 FEMSRE 713 1-5-01 270 I.B. Naumova et al. / FEMS Microbiology Reviews 25 (2001) 269^283 5.4. The Nocardiopsis alba species group . .................................. 274 6. Application of wall teichoic acid composition in taxonomy of the genus Nocardiopsis .... 276 6.1. Structures of cell wall teichoic acids and their combinations are chemical markers of intrageneric taxa . ................................................. 276 6.2. Di¡erentiating characteristics of Nocardiopsis species and subspecies based on the products of chemical degradation of cell wall teichoic acids . .................. 277 7. 13C NMR spectra of teichoic acids are indicative of intrageneric taxa of the genus Nocar- diopsis ............................................................... 278 7.1. 13C NMR spectra of teichoic acids of the N. dassonvillei subspecies . ............. 278 7.2. 13C NMR spectrum of teichoic acid of N. trehalosi .......................... 278 7.3. 13C NMR spectrum of teichoic acid of N. tropica ........................... 280 7.4. 13C NMR spectra of teichoic acids of the N. alba group ...................... 280 8. Conclusion ........................................................... 280 Acknowledgements . ...................................................... 281 References ............................................................... 281 1. Introduction more focused identi¢cation of new organisms at di¡erent taxonomic levels. The past decade has witnessed an extraordinary increase Teichoic acids are anionic carbohydrate-containing pol- in methodological approaches towards bacterial system- ymers, which occur in many Gram-positive bacteria and atics, including the introduction of rapid sequence proto- are associated with the cytoplasmic membrane (lipotei- cols for the analysis of RNA and DNA allowing the de- choic acids) [10] or covalently linked by phosphodiester termination of relationships between prokaryotic bridges to muramic acid residues in peptidoglycan (cell organisms. However, due to di¡erences in the tempo and wall teichoic acids) [11]. The possible application of lipo- mode of gene and protein evolution that exist between teichoic acids in bacterial taxonomy has been discussed organisms, the phylogenetic branching pattern of bacterial previously [10]. The data on the cell wall teichoic acids lineages per se cannot be used to de¢ne hierarchical clas- accumulated by now for Gram-positive bacteria, mainly si¢cations. Additional information is needed to facilitate actinomycetes, have demonstrated their potential for bac- the delineation of genera, species and higher taxa at the terial systematics [12^15]. phenetic level and to meet the demands of both phyloge- The physiological role of teichoic acids is thought to be netic coherence and the requirement for common pheno- in ion exchange and control of the activity of autolytic typic characters necessary for unambiguous description of enzymes that, in turn, are important for growth and divi- bacterial taxa and reliable identi¢cation of their members. sion of the bacterial cell [16]. Teichoic acids may constitute Large molecules and polymers of cells and cell enve- 60% of the cell wall and are essential for the normal func- lopes have contributed signi¢cantly to an improved classi- tioning of the bacterial cell, which spends a signi¢cant ¢cation of the order Actinomycetales embracing a large amount of energy on the synthesis of these polymers. group of Gram-positive bacteria of immense physiological, About 10 genes were shown to be involved in the control biochemical and morphological diversity, which are well of the synthesis of glycosylated poly(glycerol phosphate) known for their capacity to produce antibiotics and other teichoic acid in Bacillus sp. and of an oligomeric unit link- biologically active substances [1]. However, the limited ing this polymer to peptidoglycan [17^19]. The cell dis- number of the traditionally used chemotaxonomic charac- plays a morphological abnormality when the content of teristics based on these cell constituents, i.e., cell wall che- this polymer in the cell wall is below the norm, and mu- motype [2,3], phospholipid type [4], menaquinone [5] and tant bacilli lacking teichoic acids are not found, since they fatty acid composition [6], presence and type of mycolic appear to be unviable [16]. Other functions of these poly- acids [7], often does not provide su¤cient markers for mers are related to phage binding [20] and immunogenicity phenetic delineation of the actinomycete taxa newly de- [21]. scribed or revised mainly on the basis of phylogenetic The involvement of cell wall teichoic acids in vital cell data. There is also a special problem of reliable description functions and their great structural diversity (see below), and di¡erentiation of bacterial species in accordance with expressed by the information coded in various genes, as the current bacterial species de¢nition [8]. On the other well as their wide occurrence in Gram-positives, suppose a hand, many cell polymers and molecules have still not correlation of these polymers with other taxonomic prop- been determined or evaluated for their taxonomic value erties and suggest their applicability to the systematics of [9]. Their characterization from the taxonomic standpoint the respective microorganisms. could provide new tools for bacterial classi¢cation and a The occurrence of cell wall teichoic acids cannot be FEMSRE 713 1-5-01 I.B. Naumova et al. / FEMS Microbiology Reviews 25 (2001) 269^283 271 predicted from the phylogenetic position of taxa but, if hydrolysates). Subsequently,