Precise Species Identification for Enterobacter: a Genome Sequence-Based Study with Reporting of Two Novel Species, Enterobacter quasiroggenkampii sp. nov. and Enterobacter quasimori sp. nov

Abstract

The genus Enterobacter comprises common pathogens and has a complicated taxonomy. Precise taxonomic assignation lays a foundation for microbiology. In this study, we updated the Enterobacter taxonomy based on robust genome analyses. We found that all Enterobacter subspecies assignments were incorrect. Enterobacter cloacae subsp. dissolvens and Enterobacter hormaechei subsp. hoffmannii are species (Enterobacter dissolvens and Enterobacter hoffmannii, respectively) rather than subspecies. Enterobacter xiangfangensis, Enterobacter hormaechei subsp. oharae, and Enterobacter hormaechei subsp. steigerwaltii are not Enterobacter hormaechei subspecies but belong to the same species (Enterobacter xiangfangensis). Enterobacter timonensis should be removed to Pseudenterobacter, a novel genus. We then reported two novel species, Enterobacter quasiroggenkampii and Enterobacter quasimori, by genome- and phenotype-based characterization. We also applied the updated taxonomy to curate 1,997 Enterobacter genomes in GenBank. Species identification was changed following our updated taxonomy for the majority of publicly available strains (1,542, 77.2%). The most common Enterobacter species was E. xiangfangensis We identified 14 novel tentative Enterobacter genomospecies. This study highlights that updated and curated taxonomic assignments are the premise of correct identification.IMPORTANCE Enterobacter species are major human pathogens. Precise species identification lays a foundation for microbiology, but the taxonomy of Enterobacter is complicated and confusing. In this study, first, we significantly updated the taxonomy of Enterobacter by rigorous genome analyses and found that all subspecies assignments of Enterobacter were incorrect. Second, we characterized and reported two novel Enterobacter species with clinical significance. Third, we curated 1,997 Enterobacter genome sequences deposited in GenBank and found that the species identification of most Enterobacter strains needed to be corrected. Fourth, we found that the most common Enterobacter species seen in clinical samples is Enterobacter xiangfangensis rather than Enterobacter cloacae Fifth, we identified 14 tentative novel Enterobacter and 18 tentative novel non-Enterobacter species. This study highlights that updated and curated taxonomic assignments are the premise of correct species identification. We recommend that future Enterobacter studies need to use the updated taxonomy to avoid misleading information.

Keywords: Enterobacter; Enterobacter cloacae; Enterobacter quasimori; Enterobacter quasiroggenkampii; Enterobacteriaceae; taxonomy.

FIG 1

A phylogenetic tree based on the concatenated nucleotide sequence of core genes of Enterobacter quasimori strain 090044^T, Enterobacter quasiroggenkampii strains WCHECL1060^T and 090040, non-Enterobacter tentative taxons A to T, Enterobacter tentative taxons 1 to 14, and type strains of the family Enterobacteriaceae (listed in Data Set S1). Strains and their nucleotide accession numbers are listed alongside the species names. For species and subspecies with names that need to be revised as suggested in this study, the revised names are shown first, and the current names are shown after the slash. The tree was inferred using the maximum likelihood method under the GTRGAMMA model with a 1,000-bootstrap test, and branches with support over 50% are indicated by gradients. Bar, value indicates the nucleotide substitutions per site.

FIG 2

A more precise phylogenetic tree based on the concatenated nucleotide sequence of core genes of tentative taxons and type strains of genera Enterobacter, Leclercia, and Lelliottia (listed in Tables 5 and 7 and Data Set S1). Strains and their nucleotide accession numbers are listed alongside the names of species. For species and subspecies with names that need to be revised as suggested in this study, the revised names are shown first, and the current names are shown after the slash. The tree was inferred using the maximum likelihood method under the GTRGAMMA model with a 1,000-bootstrap test, and branches with support over 50% are indicated by gradients. Bar, value indicates the nucleotide substitutions per site.