Phylogeny Trumps Chemotaxonomy: A Case Study Involving Turicella otitidis

Abstract

The genus Turicella was proposed to harbor clinical strains isolated from middle-ear fluids of patients with otitis media. 16S rRNA phylogeny showed that it belonged to the mycolic acid-containing actinobacteria, currently classified in the order Corynebacteriales, and was closely related to the genus Corynebacterium. A new genus was proposed for the organisms as unlike corynebacteria they lacked mycolic acids and had different menaquinones. Here, we carried out large-scale comparative genomics on representative strains of the genera Corynebacterium and Turicella to check if this chemotaxonomic classification is justified. Three genes that are known to play an essential role in mycolic acid biosynthesis were absent in Turicella and two other mycolate-less Corynebacterium spp., explaining the lack of mycolic acids resulted from the deletion of genes and does not confer any phylogenetic context. Polyphasic phylogenetic analyses using 16S rRNA, bacterial core genes and genes responsible for synthesizing menaquinones unequivocally indicate that Turicella is a true member of the genus Corynebacterium. Here, we demonstrate that menaquinone and mycolic acid that have been used as critical taxonomic markers should be interpreted carefully, particularly when genome-based taxonomy is readily available. Based on the phylogenetic analysis, we propose to reclassify Turicella otitidis as Corynebacterium otitidis comb. nov.

The Mycobacterial Cell Envelope: A Relict From the Past or the Result of Recent Evolution?

“…Turicella otitidis possesses almost none of the genes involved in MA biosynthesis (see “ ∗ ” in Figure 2 ). This species is clearly in the order Corynebacteriales based on its genome sequence ( Baek et al, 2018 ). However, a recent study suggests that the genome of T. otitidis has lost the key genes involved in MA synthesis ( Baek et al, 2018 ).…”

“…This species is clearly in the order Corynebacteriales based on its genome sequence ( Baek et al, 2018 ). However, a recent study suggests that the genome of T. otitidis has lost the key genes involved in MA synthesis ( Baek et al, 2018 ). This result corroborates the fact that this bacterium does not produce MAs which is exceptional for a bacterium of the order Corynebacteriales and this microevolution has made its positioning within this order rather difficult ( Funke et al, 1994 ).…”

Corynebacterium godavarianum Jani et al. 2018 and Corynebacterium hadale Wei et al. 2018 are both later heterotypic synonyms of Corynebacterium gottingense Atasayar et al. 2017, proposal of an emended description of Corynebacterium gottingense Atasayar et al. 2017

“…These types of features (m-DAP, polar lipid types and presence of shorter length mycolates), were consistent for the genus Corynebacterium [14]. Whole genome sequences were assessed for the presence of mycolate synthesis pathway genes by using blastX to find matches for a locally built blast database comprising mycolate synthesis proteins from Corynebacterium diphtheriae and C. glutamicum (accD4, pks, cmrA, fad2, MmplM3) acquired from GenBank and Uniprot (data not shown) [6,15,16]. Homologies ranging from 62 to 78 % were found among the proteins studied, confirming the presence of mycolic acids in all strains studied.…”

“…Four Canadian isolates were described as being lipophilic (NML 99-0020, NML 00-0156, NML150383, NML180780) and three strains (NML 92-0415, NML 930607, NML120412) which grew more robustly, were not. The genome of each study strain was assessed here for the presence of the fatty acid synthase gene (fas) of the FAS-I pathway, whereby the absence of such genes was associated with Corynebacterium species which were unable to produce lipids endogenously [15]. The four lipophilic NML strains did not have the fatty acid synthase gene present but the fas gene was detected for C. gottingense, C. hadale and for the three remaining NML strains; C. godavarianum, which had been described by Jani et al as being lipophilic [2], but the fas gene was detected in this study.…”

Reviewing the Pathogenic Potential of the Otitis-Associated Bacteria Alloiococcus otitidis and Turicella otitidis

“…T. otitidis is a Gram positive bacillus; catalase positive, oxidase negative and aerobic (Funke et al, 1994). Like A. otitidis, T. otitidis is the only member of its genus and was placed in the Corynebacteriaceae family with its closest relative, Corynebacterium (Goodfellow et al, 2012); though it has recently been proposed that T. otitidis is a true member of the Corynebacterium genus (Baek et al, 2018). Like A. otitidis, T. otitidis' closest relative is also a nasopharyngeal commensal, and Corynebacterium and Dolosigranulum commonly co-occur in healthy children (Biesbroek et al, 2014;Lappan et al, 2018).…”