Genome-Based Taxonomic Classification of the Phylum
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ORIGINAL RESEARCH published: 22 August 2018 doi: 10.3389/fmicb.2018.02007 Genome-Based Taxonomic Classification of the Phylum Actinobacteria Imen Nouioui 1†, Lorena Carro 1†, Marina García-López 2†, Jan P. Meier-Kolthoff 2, Tanja Woyke 3, Nikos C. Kyrpides 3, Rüdiger Pukall 2, Hans-Peter Klenk 1, Michael Goodfellow 1 and Markus Göker 2* 1 School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, United Kingdom, 2 Department Edited by: of Microorganisms, Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Martin G. Klotz, Germany, 3 Department of Energy, Joint Genome Institute, Walnut Creek, CA, United States Washington State University Tri-Cities, United States The application of phylogenetic taxonomic procedures led to improvements in the Reviewed by: Nicola Segata, classification of bacteria assigned to the phylum Actinobacteria but even so there remains University of Trento, Italy a need to further clarify relationships within a taxon that encompasses organisms of Antonio Ventosa, agricultural, biotechnological, clinical, and ecological importance. Classification of the Universidad de Sevilla, Spain David Moreira, morphologically diverse bacteria belonging to this large phylum based on a limited Centre National de la Recherche number of features has proved to be difficult, not least when taxonomic decisions Scientifique (CNRS), France rested heavily on interpretation of poorly resolved 16S rRNA gene trees. Here, draft *Correspondence: Markus Göker genome sequences of a large collection of actinobacterial type strains were used to infer [email protected] phylogenetic trees from genome-scale data using principles drawn from phylogenetic †These authors have contributed systematics. The majority of taxa were found to be monophyletic but several orders, equally to this work families, and genera, as well as many species and a few subspecies were shown to be in need of revision leading to proposals for the recognition of 2 orders, 10 families, and 17 Specialty section: This article was submitted to genera, as well as the transfer of over 100 species to other genera. In addition, emended Evolutionary and Genomic descriptions are given for many species mainly involving the addition of data on genome Microbiology, size and DNA G+C content, the former can be considered to be a valuable taxonomic a section of the journal Frontiers in Microbiology marker in actinobacterial systematics. Many of the incongruities detected when the Received: 31 January 2018 results of the present study were compared with existing classifications had been Accepted: 09 August 2018 recognized from 16S rRNA gene trees though whole-genome phylogenies proved to be Published: 22 August 2018 much better resolved. The few significant incongruities found between 16S/23S rRNA Citation: and whole genome trees underline the pitfalls inherent in phylogenies based upon single Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, gene sequences. Similarly good congruence was found between the discontinuous Kyrpides NC, Pukall R, Klenk H-P, distribution of phenotypic properties and taxa delineated in the phylogenetic trees though Goodfellow M and Göker M (2018) Genome-Based Taxonomic diverse non-monophyletic taxa appeared to be based on the use of plesiomorphic Classification of the Phylum character states as diagnostic features. Actinobacteria. Front. Microbiol. 9:2007. Keywords: G+C content, genome size, Genome BLAST Distance Phylogeny, chemotaxonomy, morphology, doi: 10.3389/fmicb.2018.02007 phylogenetic systematics, phylogenomics Frontiers in Microbiology | www.frontiersin.org 1 August 2018 | Volume 9 | Article 2007 Nouioui et al. Classification of Actinobacteria INTRODUCTION Actinobacteria, as shown in Bergey’s Manual of Systematic Bacteriology (Goodfellow et al., 2012a). Despite the success of 16S Prokaryotic systematics is the study of the kinds and diversity rRNA gene sequencing in providing the phylogenetic backbone of Archaea and Bacteria and relationships within and between for the classification of prokaryotes (Brenner et al., 2005a; them. It encompasses the related disciplines of classification, Ludwig and Klenk, 2005) problems remain in circumscribing nomenclature and identification, the concept of the taxonomic actinobacterial taxa, including at family and genus levels. trinity (Cowan, 1955). Classification and identification are Nocardiaceae (Castellani and Chalmers, 1919), for instance, core scientific disciplines that are practiced by few but their encompass the type genus Nocardia as well as Gordonia, Millisia, applications are relevant to most, if not all, of the microbiological Rhodococcus, Skermania, and Smaragdicoccus (Goodfellow, community. Nomenclature is also central to all aspects of 2012a) though a case was also made for the continued microbiology as it deals with the correct use of names recognition of Gordoniaceae (Stackebrandt et al., 1997) to by following rules embodied in the International Code of include not only the type genus, Gordonia, but also Millisia, Nomenclature of Prokaryotes, notably the nomenclatural type Skermania, and Williamsia (Goodfellow, 2012a). Other families concept and the requirement to deposit type strains in two public considered to be problematic include Cellulomonadaceae, culture collections in different countries (Stackebrandt et al., Dermacoccaceae, Dermatophilaceae, Intrasporangiaceae, and 2014; Parker et al., 2015). Classification and identification are Nocardioidaceae (Goodfellow, 2012a). The current assignment of markedly data-dependent and thereby in a perpetual state of genera to such families should be seen as staging posts to better development driven by new taxonomic concepts and practices. classifications. Early classification of prokaryotes, including actinomycetes, The situation at the genus level is not dissimilar to that which are now known as actinobacteria, was based on outlined above as 16S rRNA gene trees often also lack the morphology and a few biochemical and physiological properties, resolution to distinguish between closely related genera, as shown as exemplified by Nocardia, the oldest name in current use for by Lechevalieria (Labeda et al., 2001) and Lentzea (Yassin et al., an aerobic actinomycete genus (Lechevalier, 1976). However, 1995), which are difficult to distinguish when assigning new the subsequent application of chemotaxonomic, molecular species to either genus (Okoro et al., 2010; Idris et al., 2017). In systematic and numerical taxonomic procedures (Goodfellow turn, the observation that Kitasatospora (Omura et al., 1982) and et al., 1985) showed that classifications dependent on form and Streptacidiphilus (Kim et al., 2003) fall within the Streptomyces function tended to result in the delineation of heterogeneous 16S rRNA gene tree led some to question their taxonomic status taxa. Nocardia, for instance, as morphologically defined in the (Kämpfer, 2012a). Along the same lines, the monospecific genera eighth edition of Bergey’s Manual of Determinative Bacteriology Jiangella (Song et al., 2005), Plantactinospora (Qin et al., 2009a), (McClung, 1974) contained species that were later assigned and Polymorphospora (Tamura et al., 2006) were interspersed taxonomically to diverse genera, including Actinomadura, within the Micromonospora 16S rRNA gene tree together with Amycolatopsis, Oerskovia, Rhodococcus, and Rothia (Goodfellow authentic representatives of Salinispora (Maldonado et al., and Minnikin, 1977; Lechevalier et al., 1986). Similarly, a series 2005) and Verrucosispora (Rheims et al., 1998) in a recent of more broadly based studies showed that coryneform bacteria, study (Trujillo et al., 2014). It is also difficult to unravel the at the time an ill-assorted group in search of a taxonomic home, internal structure of complex actinobacterial genera using data were actinomycetes (Bousfield and Callely, 1978). Conversely, acquired from polyphasic taxonomic studies, notable examples Thermoactinomyces, which had, long been classified with the include Actinomyces (Schaal and Yassin, 2012a), Amycolatopsis actinomycetes, was found to be related to aerobic, endospore- (Tan and Goodfellow, 2012), Arthrobacter (Busse et al., 2012), forming bacilli (Cross and Unsworth, 1981). Micromonospora (Carro et al., 2018), Nocardioides (Evtushenko The new advances, especially in molecular systematics, led et al., 2012), Rhodococcus (Jones and Goodfellow, 2012), and to the view that classifications at all levels in the taxonomic Streptomyces (Labeda et al., 2012). Polyphasic studies as currently hierarchy should be based on the integrated use of genotypic conducted largely depend on the 16S rRNA gene (Montero- and phenotypic data (Wayne et al., 1987; Stackebrandt, 1992). Calasanz et al., 2017) but despite its usefulness for resolving This approach, known as polyphasic taxonomy (Colwell, 1970), taxonomic questions in the past, the gene contains only a limited has become the lodestone of prokaryotic systematics (Vandamme number of characters and thus, much like any other single gene, et al., 1996; Gillis et al., 2005; Kämpfer and Glaeser, 2012). can yield trees with many statistically unsupported branches Methods selected for polyphasic studies tend to be somewhat (Klenk and Göker, 2010; Breider et al., 2014). subjective as they reflect the biology of taxa under study There is clearly a compelling need to develop an improved and available facilities. However, a prevailing theme in such framework for the classification of actinobacteria, a goal