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The Species Concept for Prokaryotes

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The Species Concept for Prokaryotes View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by MPG.PuRe FEMS Microbiology Reviews 25 (2001) 39^67 www.fems-microbiology.org Review The species concept for prokaryotes Ramon Rossello¨-Mora *, Rudolf Amann Department of Molecular Ecology, Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany Received 4 November 1999; received in revised form 23 August 2000; accepted 24 August 2000 Abstract The species concept is a recurrent controversial issue that preoccupies philosophers as well as biologists of all disciplines. Prokaryotic species concept has its own history and results from a series of empirical improvements parallel to the development of the techniques of analysis. Among the microbial taxonomists, there is general agreement that the species concept currently in use is useful, pragmatic and universally applicable within the prokaryotic world. However, this empirically designed concept is not encompassed by any of the, at least, 22 concepts described for eukaryotes. The species could be described as `a monophyletic and genomically coherent cluster of individual organisms that show a high degree of overall similarity in many independent characteristics, and is diagnosable by a discriminative phenotypic property'. We suggest to refer it as a phylo-phenetic species concept. Here, we discuss the validity of the concept in use which we believe is more pragmatic in comparison with those concepts described for eukaryotes. ß 2001 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. Keywords: Species concept; Phenetic analysis; Phylogenetic reconstruction; DNA^DNA similarity Contents 1. Introduction .......................................................... 40 2. The development of prokaryote taxonomy . .................................. 41 3. Methods and parameters used in prokaryotic species circumscription . ............. 43 3.1. Retrieving genomic information . ....................................... 43 3.2. Phenotypic methods ................................................. 48 4. Species concepts for eukaryotes ............................................ 51 5. The prokaryotic species concept ............................................ 52 5.1. The concept ...................................................... 52 5.2. The limits . ...................................................... 53 5.3. The 16S rRNA sequence data . ....................................... 53 5.4. Infraspeci¢c subdivisions . ............................................ 54 5.5. Prokaryotic sex . ................................................. 56 5.6. Pure cultures and the culture collections ................................. 56 5.7. The species concept to be used for prokaryotes ............................ 57 5.8. The phylo-phenetic species concept . .................................. 59 5.9. Guidelines to the recognition of a prokaryotic species ....................... 60 5.10. Future species circumscriptions . ....................................... 60 Acknowledgements . ...................................................... 61 References ............................................................... 61 Glossary . ................................................................ 65 * Corresponding author. Present address: Laboratori de Microbiologia, Departament de Biologia, Facultat de Cie©ncies, Universitat de les Illes Balears, Crtra. Valldemossa Km 7, 5, E-07071 Palma de Mallorca, Spain. Tel.: +34 971173140; Fax: +34 971173184; E-mail: [email protected] 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)00040-1 FEMSRE 692 29-12-00 Cyaan Magenta Geel Zwart 40 R. Rossello¨-Mora, R. Amann / FEMS Microbiology Reviews 25 (2001) 39^67 1. Introduction their diversity and importance has always been underesti- mated by non-microbiologists (Table 2). One of the rea- `The true taxonomist is a man with a mission; he often sons is that to date less than 5000 prokaryotic species have leads a cloistered life, protected from the vexations and been described. This relative low number is caused by the frustrations of the everyday world, and he may well wear problems encountered for the isolation of microorganisms blinkers as opaque as any worn by a horseT. Living a life of in pure cultures and their characterization. Problems such seclusion, safe in his small laboratory, and surrounded by his as hitherto unculturability, lack of proper research funding books, his microscope (and perhaps his computer tape), he and in some cases the underestimation of the isolation a¡ects an unconcern for the mundane application of his e¡orts are responsible for such numbers. However, the work' [1]. isolation of an organism in pure culture is to date an With these words, S.T. Cowan, one of the most avant- indispensable requisite for the recognition of prokaryotic gardist and successful taxonomists, described a not very species [4]. On the other hand, it is of general knowledge optimistic view of his own collective. However, most of among microbiologists that there is a large potential of the taxonomists would agree that today's specialist is a prokaryote diversity made up of hitherto uncultured mi- much more dynamic scientist adapted to the rush of tech- croorganisms [5^8]. Molecular techniques, most notably nical development, actively incorporating new methodolo- those based on 16S rRNA, which are directed towards gies, open for discussions, and aware that this ¢eld of analyzing community composition of environmental sam- science is slowly being taken more seriously. Microbiology ples indicate that the hitherto classi¢ed prokaryotic species itself is developing and diversifying enormously. One of account for a very small portion of the real prokaryote the `missions' of the microbial taxonomists is to create a diversity [9]. Thus, if we only take into account the recog- common language for all microbiologists. nized prokaryotic species for diversity calculations, their It is surprising, particularly for non-microbiologists, total number would never be regarded as a signi¢cant that prokaryotes, most of which are invisible to the human proportion of the total Earth's biodiversity. This under- eye, constitute an essential component of the Earth's bio- estimation of the real prokaryote diversity has obvious ta. They catalyze unique and indispensable transforma- negative e¡ects on the distribution of research funding tions in the biogeochemical cycles of the biosphere, pro- [10,11]. duce important components of the Earth's atmosphere, The species concept for prokaryotes has been developed and represent a large proportion of life's genetic diversity. in parallel to the design of laboratory techniques that per- In contrast to textbook knowledge, the estimated mitted the retrieval of useful information. The original 4^6U1030 prokaryotic cells existing on the Earth (Table species concepts based on morphological traits were dem- 1) might even constitute s 50% of the protoplastic bio- onstrated to be wrongly tailored. Improved concepts have mass (excluding most of the plant biomass that is made up developed through the use of new information units (e.g. of extracellular material such as cell walls and structural chemotaxonomic markers, DNA properties, rRNA se- polymers [2]). It is also interesting to note that the major- quencesT). At the present, many, if not all, prokaryote ity of the prokaryotes may be located in oceanic and ter- taxonomists agree that the current species circumscription, restrial subsurface environments. Less attention than those although not perfect, is acceptable and pragmatic, and of the Earth's surface has been paid to these habitats. covers the primary goals of taxonomy such as a rapid Thus, research in microbiology might have dealt with a and reliable identi¢cation of strains [12]. However, among very small portion of the total Earth's prokaryotic com- non-taxonomists, the prokaryotic species concept is munity. criticized. For some, the concept is too conservative, lead- Several attempts to estimate the number of species living ing to an underestimation of the real prokaryote diversity on Earth have been made, and it seems that the number of [2,13]. They consider the conservative nature of the con- recorded species is directly related to the e¡ort and interest cept to be a signi¢cant disadvantage in as much as it is not of the scientists [3]. However, in spite of the enormous comparable to the concepts designed for higher eukaryotes quantitative contribution of prokaryotes to the biosphere, [14,15]. The current discussion about the adequacy of the Table 1 Number and biomass of prokaryotes in the world (data obtained from [2]) Environment No. of prokaryotic cells (U1028)gofC(U1015) Aquatic habitats 12 2.2 Oceanic subsurface 355 303 Soil 26 26 Terrestrial subsurface 25^250 22^215 Total 415^640 353^546 Plantsa ^ 562 aPlant carbon is the sum of protoplastic biomass, structural polymers and cell wall material. FEMSRE 692 29-12-00 Cyaan Magenta Geel Zwart R. Rossello¨-Mora, R. Amann / FEMS Microbiology Reviews 25 (2001) 39^67 41 Table 2 a systematic arrangement of microorganisms [18]. He cre- Estimates on the contribution of major groups of organisms to the total ated two form genera, Monas and Vibrio, which encom- biological diversity [16] passed bacteria and di¡erentiated the punctiform and the Organism Percent of contribution elongated
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