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International Journal of Systematic and Evolutionary Microbiology (2016), 66, 5575–5599 DOI 10.1099/Ijsem.0.001485

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International Journal of Systematic and Evolutionary Microbiology (2016), 66, 5575–5599 DOI 10.1099/Ijsem.0.001485 International Journal of Systematic and Evolutionary Microbiology (2016), 66, 5575–5599 DOI 10.1099/ijsem.0.001485 Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Mobolaji Adeolu,† Seema Alnajar,† Sohail Naushad and Radhey S. Gupta Correspondence Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Radhey S. Gupta L8N 3Z5, Canada [email protected] Understanding of the phylogeny and interrelationships of the genera within the order ‘Enterobacteriales’ has proven difficult using the 16S rRNA gene and other single-gene or limited multi-gene approaches. In this work, we have completed comprehensive comparative genomic analyses of the members of the order ‘Enterobacteriales’ which includes phylogenetic reconstructions based on 1548 core proteins, 53 ribosomal proteins and four multilocus sequence analysis proteins, as well as examining the overall genome similarity amongst the members of this order. The results of these analyses all support the existence of seven distinct monophyletic groups of genera within the order ‘Enterobacteriales’. In parallel, our analyses of protein sequences from the ‘Enterobacteriales’ genomes have identified numerous molecular characteristics in the forms of conserved signature insertions/deletions, which are specifically shared by the members of the identified clades and independently support their monophyly and distinctness. Many of these groupings, either in part or in whole, have been recognized in previous evolutionary studies, but have not been consistently resolved as monophyletic entities in 16S rRNA gene trees. The work presented here represents the first comprehensive, genome- scale taxonomic analysis of the entirety of the order ‘Enterobacteriales’. On the basis of phylogenetic analyses and the numerous identified conserved molecular characteristics, which clearly distinguish members of the order ‘Enterobacteriales’ and the seven reported clades within this order, a proposal is made here for the order Enterobacterales ord. nov. which consists of seven families: Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. INTRODUCTION Members of this group inhabit a number of different ecologi- cal niches and have been found in soil, water and in associa- The order ‘Enterobacteriales’ is a large and diverse group of tion with living organisms including plants, insects, animals Gram-negative, facultatively anaerobic, non-spore-forming, and humans (Brenner & Farmer, 2005). Many members of rod-shaped bacteria within the class Gammaproteobacteria. the order ‘Enterobacteriales’ have been implicated as pathogens in humans and animals, such as the species Escherichia coli, Salmonella enterica, and Yersinia pestis, and as economically †These authors contributed equally to this work. devastating phytopathogens, such as members of the genera Abbreviations: CSI, conserved signature insertion/deletion; MLSA, mul- Dickeya, Pectobacterium, Brenneria, Erwinia and Pantoea tilocus sequence analysis. (Bonn & van der Zwet, 2000; Coutinho & Venter, 2009; Seventy-five supplementary figures and five supplementary tables are Croxen & Finlay, 2010; Hauben et al., 1998; Livermore, 2012; available with the online Supplementary Material. Tyler & Triplett, 2008). At the time of writing, the order 001485 ã 2016 IUMS Printed in Great Britain 5575 M. Adeolu and others ‘Enterobacteriales’ contains 60 genera with validly published (Ee et al., 2016), and, most commonly, the genes gyrB, rpoB, names (www.namesforlife.com; Parte, 2014) including the atpD and infB (Brady et al., 2008, 2013, 2014b; Glaeser & recently described genus Chania (Ee et al., 2016) and an addi- K€ampfer, 2015; Zhang & Qiu, 2015). These studies have led tional genus which has been recently described but the name to a significant number of reclassifications within the order is not yet validly published [‘Atlantibacter’ (Hata et al., 2016)]. ‘Enterobacteriales’ and have alleviated many of the issues Most genera within the order ‘Enterobacteriales’, encompass- related to polyphyletic genera within the order. However, no ing over 250 species, are placed within the sole family with a family-level divisions within the order ‘Enterobacteriales’ have validly published name within the order, Enterobacteriaceae; thus far been proposed. making the family Enterobacteriaceae one of the most taxo- The increasing prevalence and ubiquity of genome sequenc- nomically diverse bacterial families currently recognized ing technology has led to an increasing wealth of publically (www.namesforlife.com; Parte, 2014). A number of distinct available genome sequence data. Currently, there are over groupings of genera within the family Enterobacteriaceae are 14 000 genomes from 54 genera with valildy published names well known (viz. the groupings of the genera Salmonella, Cit- within the order ‘Enterobacteriales’ available in the NCBI robacter and Escherichia/Shigella, and the genera Dickeya, Pec- genome database (http://www.ncbi.nlm.nih.gov/genome). tobacterium and Brenneria, the close associations between the These genome sequences are enabling the increasing use of genera Xenorhabdus and Photorhabdus, the genera Erwinia robust and reliable core genome-based phylogenetic recon- and Pantoea, and the genera Obesumbacterium and Hafnia) structions in ‘Enterobacteriales’ research (Husník et al., 2011; (Goodrich-Blair & Clarke, 2007; Naushad et al., 2014; Octavia Wattam et al., 2014; Zhang & Qiu, 2015; Zhang et al., 2016), & Lan, 2014; Samuel et al., 2004; Zhang & Qiu, 2015; Zhang which have been shown to mitigate the effects of recombina- et al., 2016), but these groupings are not recognized as unique tion or lateral gene transfer and provide greater resolving taxonomic units. power than phylogenetic trees based on single genes/proteins The biochemical diversity and the large number of organisms (Ciccarelli et al., 2006; Gao et al., 2009; Rokas et al., 2003; Wu within the order ‘Enterobacteriales’ has made biochemical et al., 2009). Genome sequence data is also enabling the detec- descriptions of the order and its constituent subgroups diffi- tion of conserved molecular characteristics shared by evolu- cult (Brenner & Farmer III, 2005; Octavia & Lan, 2014). Our tionarily related groups of organisms. One particular class of current understanding of the phylogeny and interrelation- conserved molecular characteristics, which have recently been ships of the members of the order ‘Enterobacteriales’ is pri- utilized to great effect in prokaryotic taxonomy are conserved marily based on the 16S rRNA gene (Francino et al., 2006; signature insertions/deletions (CSIs) present in widely distrib- Hauben et al., 1998; Naum et al., 2008; Spröer et al., 1999). uted proteins (Gupta, 2014, 2016; Naushad et al., 2014). CSIs However, the 16S rRNA gene has low discriminatory power are insertions or deletions (indels) that are uniquely present and interrelationships of the members of the order in a related group of organisms. The most parsimonious ‘Enterobacteriales’ are poorly resolved in 16S rRNA-gene- explanation of the presence of the CSI in a related group of based phylogenetic trees (Hauben et al., 1998; Naum et al., organisms is the existence of a common ancestor in which 2008; Octavia & Lan, 2014). Additionally, the branching of the genetic change leading to the CSI occurred, and which the genera and species within ‘Enterobacteriales’ in 16S rRNA- was subsequently inherited by all of its various desce dents. gene-based phylogenies shows considerable stochasticity Thus, CSIs represent synapomorphic characteristics and they depending on the algorithms used and the organisms analysed provide reliable evidence, independent of phylogenetic trees, (Naum et al., 2008; Octavia & Lan, 2014). Most concerning, that the species from the groups in which they are found are comprehensive 16S rRNA gene phylogenetic trees for the specifically related to each other due to common ancestry. order ‘Enterobacteriales’ and other members of the class Gam- Recently, on the basis of CSIs and other molecular character- maproteobacteria suggest that the order ‘Enterobacteriales’ istics, the taxonomy of a number of important prokaryotic exhibits polyphyletic branching and does not form a coherent groups, ranging from genus to phylum level taxa, has been monophyletic grouping (Brenner & Farmer, 2005; Octavia & revised (Campbell et al., 2015; Gupta, 2016; Gupta et al., 2015a, b, 2016; Naushad et al., 2014, 2015b; Sawana et al., Lan, 2014; Yarza et al., 2008; Yilmaz et al., 2013). A number 2014). of alternative genes have been employed in phylogenetic anal- ysis of the order ‘Enterobacteriales’ in order to gain additional In our earlier work, a limited number of CSIs and unique insight into the interrelationships of the members of the proteins, referred to as conserved signature proteins, were order, such as gyrB (Dauga, 2002; Fukushima et al., 2002), identified that were distinctive characteristics of either all dnaJ (Pham et al., 2007), oriC (Roggenkamp, 2007) and recA Gammaproteobacteria or were commonly shared by mem- (Tailliez et al., 2010). More recently, multiple gene/protein- bers from certain orders of Gammaproteobacteria
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