Uncultivated microbes in need of their own taxonomy

The ISME Journal (2017) 11, 2399–2406 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 www.nature.com/ismej PERSPECTIVE Uncultivated microbes in need of their own taxonomy Konstantinos T Konstantinidis1, Ramon Rosselló-Móra2 and Rudolf Amann3 1 School of Civil and Environmental Engineering and School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA; 2Marine Microbiology Group, Institut Mediterrani d’Estudis Avançats (IMEDEA; CSIC-UIB), Esporles, Spain and 3Max Planck Institute for Marine Microbiology, Bremen, Germany The great majority of microbial species remains uncultured, severely limiting their taxonomic characterization and thus communication among scientists. Although Candidatus was devised as a provisional category to classify uncultured taxa, it has not been widely accepted owing to technical limitations and lack of priority of Candidatus names in the official nomenclature. High-throughput sequencing provides the potential for data-rich taxonomic descriptions of uncultivated microbes, comparable in quality to those of cultured organisms. In order to fully realize this potential, standards and guidelines on how to perform these descriptions are needed. Here we aimed to outline these standards and draw the roadmap for a new genome-based taxonomy that, at least initially, would be parallel but highly convergent to the one in existence for isolates. In particular, we recommend the use of DNA genome sequences, recovered by population binning or single-cell techniques, as the basis for (i) identification and phylogenetic placement, (ii) bioinformatics-based functional and thus phenotypic predictions, as well as (iii) type material. We also recommend the implementation of an independent nomenclatural system for uncultivated taxa, following the same nomenclature rules as those for cultured Bacteria and Archaea but with its own list of validly published names. If widely adopted, this system will not only facilitate a comprehensive characterization of the ‘uncultivated majority’, but also provide a unified catalogue of validly published names, thereby avoiding synonyms and confusion. We also suggest that a committee of experts, supported by an international microbiological society, should be formed to govern the new classification system. The ISME Journal (2017) 11, 2399–2406; doi:10.1038/ismej.2017.113; published online 21 July 2017 Introduction The exact number of bacterial and archaeal species (that is, the prokaryotes) on the planet remains an unresolved issue of considerable debate with estimates ranging from millions to trillions (Amann and Rossello-Mora, 2016; Locey and Lennon, 2016; Schloss et al., 2016). Yet, there is no doubt that the great majority remains unclassified as only about 13 000 species of Bacteria and Archaea have been described and their names validly published to date (http://www.bacterio.net/; Parte, 2014). This represents a major limitation for better understanding, studying and communicating about the biodiversity Correspondence: KT Konstantinidis, School of Civil and Environmental Engineering and School of Biological Sciences, Georgia Institute of Technology, 311 Ferst Drive, ES&T Building, Room 3321, Atlanta, Georgia 30332-0512, USA. E-mail: or R Rossello-Mora, Marine Microbiology Group, Institut Mediterrani d’Estudis Avançats (IMEDEA; CSIC-UIB), Esporles E-07190, Spain. E-mail: or R Amann, Max Planck Institute for Marine Microbiology, Bremen D-28359, Germany. E-mail: Received 7 February 2017; revised 18 May 2017; accepted 23 May 2017; published online 21 July 2017 on the planet. The main underlying reason is that, in recent times, the current classification has been limited to pure cultures, although the great majority of microorganisms cannot yet be cultured under laboratory settings. In fact, there is no official classification but just an official nomenclature that is ruled by the International Code of Nomenclature of Prokaryotes (ICNP; Parker et al., 2015), under the auspices of the International Committee for Systematics of Prokaryotes (ICSP). A new taxonomic name will be validly published, thus officially recognized, only if the description includes the deposition of pure cultures in two international culture collections. In the early 1990s, the development of rRNAbased molecular techniques applied to the identification and visualization of uncultured organisms promoted the establishment of a provisional taxonomic status that was called Candidatus (Murray and Schleifer, 1994; Murray and Stackebrandt, 1995). Description of a Candidatus required a 16S rRNA gene sequence assigned by a specific oligonucleotide probe to microbial cells visualized microscopically and, subsequently, further characterization by features such as morphology, Gram or other cell staining, habitat localization, unusual cellular features and a growth temperature estimate inferred from the habitat. This provisional category A taxonomy for the uncultivated majority KT Konstantinidis et al 2400 was adopted only by a few microbiologists often working with endosymbionts (for example, Collingro et al., 2005) or microorganisms with conspicuous features, such as magnetotactic bacteria (for example, Abreu et al., 2007) or giant sulfur bacteria (Salman et al., 2011). Furthermore, the Candidatus status has never been covered by the ICNP, therefore Candidatus names are not validly published and have no priority. This also means that the name would not necessarily be retained in the case of isolation and formal description of another representative of the Candidatus taxon. The lack of standing in nomenclature has discouraged scientists in establishing general standards to classify uncultured taxa and resulted in a lack of a clear record of what has been hitherto classified as Candidatus. The number of Candidatus catalogued in the List of Prokaryotic Names with Standing in the Literature (http://www. bacterio.net/index.html) is around 360, but there are certainly many additional names that have never been catalogued. The lack of standing of Candidatus in the ICNP also resulted in a lack of a nomenclatural review of the new classifications and consequently errors in the etymologies of about 30% of the names (Oren, 2016). Such errors would impede the valid publication of the corresponding taxon in the case of a formal classification once a culture is available. In addition, most of the uncultured taxa newly discovered in the past decades have not been given Linnean binominal names but just received simple alphanumeric identifiers, such as clades Ia and Ib of the surface SAR11 oceanic bacteria. These identifiers are neither descriptive of phenotypic or ecological features nor indicative of taxonomic categories, such as phylum, class, order, family, genus or species. Finally, redundant identifiers for the same taxon are common nowadays, as a regulation of the alphanumeric identifier has been lacking, causing c (...truncated)