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Background  The recent emergence and dissemination of high-level mobile tigecycline resistance Tet(X) challenge the clinical effectiveness of tigecycline, one of the last-resort therapeutic options for complicated infections caused by multidrug-resistant Gram-negative and Gram-positive pathogens. Although  tet (X) has been found in various bacterial species, less is known about phylogeographic distribution and phenotypic variance of different genetic variants.    Methods  Herein, we conducted a multiregional whole-genome sequencing study of  tet (X)-positive  Acinetobacter  isolates from human, animal, and their surrounding environmental sources in China. The molecular and enzymatic features of  tet (X) variants were characterized by clonal expression, microbial degradation, reverse transcription, and gene transfer experiments, while the  tet (X) genetic diversity and molecular evolution were explored by comparative genomic and Bayesian evolutionary analyses.    Results  We identified 193  tet (X)-positive isolates from 3846 samples, with the prevalence ranging from 2.3 to 25.3% in nine provinces in China. The  tet (X) was broadly distributed in 12  Acinetobacter  species, including six novel species firstly described here. Besides  tet (X3) ( n  = 188) and  tet (X4) ( n  = 5), two  tet (X5) variants,  tet (X5.2) ( n  = 36) and  tet (X5.3) ( n  = 4), were also found together with  tet (X3) or  tet (X4) but without additive effects on tetracyclines. These  tet (X)-positive  Acinetobacter  spp. isolates exhibited 100% resistance rates to tigecycline and tetracycline, as well as high minimum inhibitory concentrations to eravacycline (2–8 μg/mL) and omadacycline (8–16 μg/mL). Genetic analysis revealed that different  tet (X) variants shared an analogous IS CR2 -mediated transposon structure. The molecular evolutionary analysis indicated that Tet(X) variants likely shared the same common ancestor with the chromosomal monooxygenases that are found in environmental Flavobacteriaceae bacteria, but sequence divergence suggested separation ~ 9900 years ago (7887 BC), presumably associated with the mobilization of  tet (X)-like genes through horizontal transfer.    Conclusions  Four  tet (X) variants were identified in this study, and they were widely distributed in multiple  Acinetobacter  spp. strains from various ecological niches across China. Our research also highlighted the crucial role of IS CR2  in mobilizing  tet (X)-like genes between different  Acinetobacter  species and explored the evolutionary history of Tet(X)-like monooxygenases. Further studies are needed to evaluate the clinical impact of these mobile tigecycline resistance genes.    Supplementary information  The online version contains supplementary material available at 10.1186/s13073-020-00807-5.

Genetic diversity and characteristics of high-level tigecycline resistance Tet(X) in Acinetobacter species