Actinomycetes University of Udine, Mycology Department ISSN: 0732-0574 Vol. 1, Num. 3, 1990, pp. 63-66

The Population Concept In Microbiology

V.D. KUZNETSOV

Institute of Microbiology, USSR Academy of Sciences, 117811 Moscow, USSR

Code Number: AC90009
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Since the scientific basis of biological systematics of living beings was laid down by Linnaeus the concept of species has undergone numerous changes and improvements. This process continues at present reflecting the progress of biological sciences. Systematics summarise the recent advances of the latter.

While the problem of species in higher organisms is solved mainly on the basis of reproductive and geographic isolation these principles cannot be used for prokaryotes (agamic cosmopolites).

One of the first students of actinomycetes, Lieske (1921), observing the enormous variability of the organisms believed that their separation into species was impossible and suggested designating actinomycetes by numbers. Later this viewpoint was rejected. The existence of species of actinomycetes in nature was substantiated and numerous schemes for their classification created (Krassilnikov, 1941, 1949, 1970; Waksman and Lechevalier, 1953; Pridham et al., 1958; Baldacci et al., 1954; Gauze et al., 1983, etc.).

A large contribution to the systematics of the actinomycetes was made by the founder of the Russian school of actinomycetologists N.A. Krassilnikov. He formulated the principles of modern systematics of the actinomycetes based on botanical foundations and built up a hierarchic system of genera considering the relationships revealed by the method of experimental variation (Krassilnikov, 1938), described in a number of treatises (Krassilnikov, 1970; Goodfellow and Cross, 1984; Sneath, 1986).

Thus modern systematics of the actinomycetes at the generic level may be considered more or less satisfactory. This is not true of systematics at the species level, and the species is a basic systematic unit. Imperfection of species systematics can be understood if we note that the concept of microbiological species does not comprise the variation range. In other words the species concept does not take into account the notion of population.

In microbiology the species is actually identified with the so-called "type strain" which is essentially a single sample from the population of the really existing species (International Code of Nomenclature of Bacteria, Lepage, 1975). In nature species exist not as type strains but as populations comprising the "type strain" as a component of parallel series of variability (Kuznetsov, 1973). Often the "type strain" does not belong to the main variant of the population and consequently does not reflect the true (the full array) characters of the species, to say nothing of the fact that the "type strain" gives no idea of the variation range (of the population composition) of the species actually existing in nature.

The explosion of the number of species of the actinomycetes recorded in scientific literature, described as "type strains", led to contamination of systematics with nominal species. The abundance of potential nominal species in systematics not only distorts the notion of the actual species diversity of the actinomycetes but also interferes with its prognostic value, does not contribute to the elaboration of fundamental biological concepts and impedes its practical application. According to Mayr (1969) "It is one of the continuing preoccupations of the taxonomist to unmask nominal species that are not genuine biological species".

A way out of this unsatisfactory situation in species systematics of the actinomycetes, to our opinion, is the revision of existing systematics using a new approach based on the population concept of the species which may be expressed in the following terms: the species is a population of genotypically closely related but phenotypically heterogeneous variants with a quantitative basis of variants possessing the complete complex of characteristic morphocultural and physio-biochemical characters.

The new approach to the revision of systematics of the actinomycetes and to its improvement on the basis of the population concept of the species comprises the following stages of research: (a) studies of intraspecific variation, (b) classification of spontaneous variants of populations of compared cultures into parallel series, (c) comparison of morpho-cultural and physio-biochemical characters of similar variants of parallel series, (d) detection of "cross" (identical) variants in populations of cultures described earlier as the "type strains" of new species, (e) recognition of nominal species and their expurgation from systematics.

In species descriptions and redescriptions it is suggested that data be included on the composition (variation range) of their populations and on physio-biochemical and cultural morphological characters of variants composing populations.

The fruitfulness of the new approach to species systematics of the actinomycetes is confirmed by ample experimental material (Kuznetsov et al., 1978; Kuznetsov and Filippova, 1982; Sveshnikova et al., 1983).

The above may be exemplified by the data on systematic revision of the fluorescent subgroup of globisporine actinomycetes consisting according to Krassilnikov (1970) of four species: Streptomyces chrysomallus, S.fluorescens, S.galbofluorescens and S.citreofluorescens.

The comparative population analysis of all four species demonstrated (Kuznetsov and Filippova, 1982) that two of them: S.fluorescens and S.galbofluorescens are identical to spontaneous variants (pale and oligosporous smooth, respectively) of the species S. chrysomallus (Fig. l). Such variants are named "cross" ones. These variants make up only 1.2% and 1.6% of the population of S.chrysomallus while the first of them accounts for the bulk of the population of the "species" S.fluorescens (94.8%) and the second the bulk of the population of the "species" S.galbofluorescens (77%) (Fig.2). In other words these cultures are actually nominal species and should be excluded from the group of fluorescent actinomycetes.

Figure 1. Population structure of Streptomyces chrysomallus (variants)

Figure 2. "Cross variants" from the population of Streptomyces chrysomallus making a bulk of populations of the "species" S.fluorescens and S.galbofluorescens.

Thus these species described by Krassilnikov from the position of identification of the species with the "type strain" are actually spontaneous variants of S.chrysomallus described earlier.

In regard to the last representative of fluorescent streptomycetes, S.citreofluorescens is a separate species, as confirmed by the comparative population-taxonomic analysis.

The revision of species systematics of the subgroup of fluorescent streptomycetes thus demonstrated that it consists not of four but only two species: S.chrysomallus and S.citreofluorescens.

It was of interest to confirm these conclusions on the revision of species systematics of this subgroup of streptomycetes by the method of DNA-DNA hybridization. Joint studies with the Interdepartmental Laboratory of Moscow State University (T.P.Turova and T.I.Ivanova) demonstrated that the extent of hybridization of all variants of the homologous series of the S.chrysomallus population and also the so-called "type strains" of S.fluorescens and S.galbofluorescens is 75-100%, i.e. within the range of intraspecific hybridization. In the case of S.citreofluorescens the DNA hybridization does not exceed the interspecific level (55%).

This example convincingly demonstrates the inadequacy of the system based on the species concept as the "type strain" and points to the necessity of a complete revision of species systematics of the actinomycetes based on the population species concept.

As follows from disconnected published data the phenomenon of parallelism in hereditary variation may be found not only in the actinomycetes but also in other prokaryotic groups. Therefore the population species concept in all probability may be extended to the whole Prokaryotae Kingdom. It is advisable to design their species systematics on the basis of the comparative population-taxonomic analysis.

The scientific significance of the discovery of the phenomenon of parallelism (homologous series) in hereditary variation of representatives of the Prokaryotae provides a possibility of establishing relationships between particular species and groups of microorganisms, finding intermediate forms between taxa and solving problems of speciation, microevolution and population genetics. It constituted a basis not only for a new approach to species systematics of the actinomycetes, and for the population species concept in microbiology but also made it possible to improve the selection of strains producing antibiotics, to suggest models for biochemical research, for the unprejudiced evaluation of significance of chemotaxonomic properties and of the level of intra- and interspecific hybridization of DNA.

References

Baldacci, E., C.Spalla & A.Grein (1954). The classification of the Actinomyces species (Streptomyces). Arch. Microbiol., 20, 347-357.

Sneath, P.H. (ed.) (1986). Bergey's Manual of Systematic Bacteriology. Williams & Wilkins Co., Baltimore, Vol. 2, 965 pp.

Gauze, G.F.T.P. Preobrazhenskaya, M.A. Sveshnikova, L.P. Terekhova & T.S. Maksimova (1983). Key to the Actinomycetes. Nauka Publ., Moscow, 246 pp. (In Russian)

Goodfellow, M. & T.Cross (1984). Classification. In: Goodfellow M., Mordarski, M. & Williams, S.T. (eds.) The Biology of the Actinomycetes. Academic Press, London, pp. 7164

Lapage, S.P.P.H.A.Sneath, E.F.Lessel, V.B.D.Skerman, H.P.R.Seeliger & W.A. Clark (eds.) (1975). International Code of Nomenclature of Bacteria. Am. Soc. Microbiol., Washington, 180 pp.

Krassilnikov, N.A. (1938). Actinomycetales and Related Organisms. Ac. Sci. USSR Publ. Moscow-Leningrad, 328 pp. (In Russian)

Krassilnikov, N. (1941). Key to the Actinomycetales. Ac. Sci. USSR Publ., Moscow-Leningrad, 148 pp. ( In Russian)

Krassilnikov, N. (1949). Key to Bacteria and Actinomycetes. Ac. Sci. USSR Publ., Moscow-Leningrad, 830 pp. (In Russian)

Krassilnikov, N.A. (1970). The Ray Fungi. Nauka Publ., Moscow, 535 pp. (In Russian)

Kuznetsov, V.D. (1973). Homologous series in hereditary variability of the actinomycetes. Antibiotiki, 18:579- 586 (In Russian)

Kuznetsov, V.D. & S.N.Filippova (1982). Taxonomy of fluorescent streptomycetes based on comparative population analysis. Mikrobiologija, 51:823-832 (In Russian)

Kuznetsov, V.D., S.Sabirov & S.N.Filippova (1978). Studies of population composition of Actinomyces tumemacerans and A.albus var.fungatus. Mikrobiologija, 47:1073-1080 (In Russian)

Lieske, IL (1921). Morphologie und Biologie der Strahlenpilze. Leipzig

Mayr, E. (1969). Principles of Systematic Zoology. McGraw-Hill Book Co., 145 pp.

Pridham, T.G., C.W.Hesseltine & R.G. Benedict (1958). A guide for the classification of streptomycetes according to selected groups. Appl. Microbiol., 6:52-79

Sveshnikova, M., O.E.Timuk, V.N.Borisova G.B.Fedorova (1983). Streptomyces variegatus sp. nov. producing an antibiotic of the alfaoxy-keto-pentaene group. Antibiotiki, 28: 723-728 (In Russian)

Waksman, S.A. & H.A.Lechevalier (1953). Guide to the Classification and Identification of the Actinomycetes and their Antibiotics. The Williams and Wilkins Co., Baltimore, 246 pp.

Copyright 1990 C.E.T.A., The International Centre for Theoretical and Applied Ecology, Gorizia

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