Abstract:

Objective:

Due to the fact that K. variicola, K. quasipneumoniae and K. pneumoniae are closely related bacterial species, misclassification can occur due to mistakes either in normal biochemical tests or during submission to public databases. The objective of this work was to identify K. variicola and K. quasipneumoniae genomes misclassified in GenBank database.

Materials and methods:

Both rpoB phylogenies and average nucleotide identity (ANI) were used to identify a significant number of misclassified Klebsiella spp. genomes.

Results:

Here we report an update of K. variicola and K. Quasipneumoniae genomes correctly classified and a list of isolated genomes obtained from humans, plants, animals and insects, described originally as K. pneumoniae or K. variicola, but known now to be misclassified.

Conclusions:

This work contributes to recognize the extensive presence of K. variicola and K. quasipneumoniae isolates in diverse sites and samples.

Keywords:
bacterial infections; Gram-negative bacterial infections; Enterobacteriaceae infections; nitrogen fixation

Resumen:

Objetivo:

Identificar genomas mal clasificados de K. variicola, y K. quasipneumoniae en la base de datos del GenBank.

Material y métodos:

En el presente estudio se usaron tanto análisis filogenéticos usando rpoB como la identidad media de nucleótidos (ANI, por sus siglas en ingles) para identificar un número significativo de genomas del género Klebsiella.

Resultados:

Se reportó una actualización de genomas de K. variicola y K. quasipneumoniae correctamente clasificados y una lista de aquellos aislamientos obtenidos de seres humanos, plantas, animales e insectos, descritos originalmente como K. pneumoniae o K. variicola pero ahora se conoce que están mal clasificados.

Conclusiones:

Este trabajo contribuye a la presencia extensiva de aislamientos de K. variicola y K. quasipneumoniae en diversos sitios y muestras.

Palabras clave:
infecciones bacterianas; infecciones por bacterias gramnegativas; fijación de nitrógeno

Introduction

A recent taxonomic description of the genus Klebsiella spp. includes three taxonomic subspecies; K. pneumoniae subsp. pneumoniae (KpI), K. pneumoniae subsp. rhinoscleromatis and K. pneumoniae subsp. ozaenae and our novel species; Klebsiella variicola (KpIII), K. singaporensis, K. michiganensis and K. quasipneumoniae (KpII), which has two subspecies: Klebsiella quasipneumoniae subsp. quasipneumoniae (KpII-A) and K. quasipneumoniae subsp. similipneumoniae (KpII-B).¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... For these bacterial species novel genome sequences have been described from the strains 07A044, 18A0691 and FIHV2014.²2. Arena F, Henrici De Angelis L, Pieralli F, Di Pilato V, Giani T, Torricelli F, et al. Draft Genome Sequence of the First Hypermucoviscous Klebsiella quasipneumoniae subsp. quasipneumoniae Isolate from a Bloodstream Infection. Genome Announc 2015;3(5):pii: e00952-15. https://doi.org/10.1128/genomeA.00952-15
https://doi.org/10.1128/genomeA.00952-15... The misclassification of K. variicola and Klebsiella spp. genomes was first identified by whole-genome and rpoB phylogenies.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... ^,44. Hazen TH, Zhao L, Sahl JW, Robinson G, Harris AD, Rasko DA, et al. Characterization of Klebsiella sp. strain 10982, a colonizer of humans that contains novel antibiotic resistance alleles and exhibits genetic similarities to plant and clinical Klebsiella isolates. Antimicrob Agents Chemother 2014;58(4):1879-1888. https://doi.org/10.1128/AAC.01605-13
https://doi.org/10.1128/AAC.01605-13... Subsequently by K. quasipneumoniae and other K. variicola genomes the misclassification was evidenced by Average Nucleotide Identity (ANI).⁵5. Chen M, Li Y, Li S, Tang L, Zheng J, An Q. Genomic identification of nitrogen-fixing Klebsiella variicola, K. pneumoniae and K. quasipneumoniae. J Basic Microbiol 2016;56(1):78-84. https://doi.org/10.1002/jobm.201500415
https://doi.org/10.1002/jobm.201500415... The aim of this work was detect misclassified K. variicola and K. quasipneumoniae genomes. We used an rpoB gene phylogenetic analysis and the results were validated by ANI. We identified the isolates misclassified previously described5 and identified new isolates that corresponded to K. variicola and K. quasipneumoniae that were deposited as K. pneumoniae. Likewise, we identified one K. variicola genome misclassified that corresponds to K. quasipneumoniae subsp. similipneumoniae.

Materials and methods

Identification of the K. variicola and K. quasipneumoniae genomes

The complete nucleotide sequence of rpoB (KVR801 v1_470024) gene from K. variicola 801 (CDMV00000000) was downloaded from the European Nucleotide Archive database.⁶6. European Nucleotide Archive. ENA.[cited 2016 Jan]. Available from: http://www.ebi.ac.uk/ena
http://www.ebi.ac.uk/ena... The rpoB sequence was analyzed by the BLASTn option (with default values) against 419 complete and draft Klebsiella spp. (tax id: 570) genomes deposited in GenBank database (last analysis 13/07/2015).⁷7. National Library of Medicine. Basic Local Alignment Search Tool (BLAST) [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information [cited 2016 Jan]. Available from: https://blast.ncbi.nlm.nih.gov/Blast.cgi
https://blast.ncbi.nlm.nih.gov/Blast.cgi... The rpoB genes from Escherichia coli K-12-MG1655, Salmonella enterica Ty21a, Klebsiella oxytoca KCTC1686, K. quasipneumoniae subsp. quasipneumoniae 18A069 (KpII-A), K. quasipneumoniae subsp. quasipneumoniae 01A030 (KpII-A) and K. quasipneumoniae subsp. similipneumoniae 07A044 (KpII-B) genomes¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... were included in the phylogenetic analysis. Subsequently, the rpoB nucleotide sequences of K. pneumoniae genomes with 100% nucleotide identity were filtered out to exclude a possible bias. All strain genomes identified as K. variicola and K. quasipneumoniae were included. Finally, a phylogenetic reconstruction was performed using the maximum-likelihood method with a Tamura-Nei-parameter model and 1000 bootstrap replications (Mega v6.06).⁸8. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011;28(10):2731-2739. https://doi.org/10.1093/molbev/msr121
https://doi.org/10.1093/molbev/msr121...

The ANI was determined using the Average Nucleotide Identity Calculator⁹9. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007;57(Pt 1):81-91 [cited 2016 January]. Available from: http://enve-omics.ce.gatech.edu/ani/
from: http://enve-omics.ce.gatech.edu/an... the default parameters. In total, thirty-one K. variicola, nine K. quasipneumoniae and two K. pneumonia genomes were downloaded from GenBank and analyzed (table I). K. variicola At-22 (CP001891), K. quasipneumoniae subsp. quasipneumoniae 18A069 (CBZM000000000), K. quasipneumoniae subsp. similipneumoniae 07A044 (CBZR000000000) and K. pneumoniae MGH78578 (CP000647) were used as reference genomes of the respective bacterial species.

Results and discussion

Klebsiella spp. genomes that corresponded to K. variicola and K. quasipneumoniae

Both K. variicola as K. pneumoniae and K. quasipneumoniae isolates exhibit very similar biochemical features,¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... and to date there are no reported biochemical tests for their appropriate differentiation.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... ^,44. Hazen TH, Zhao L, Sahl JW, Robinson G, Harris AD, Rasko DA, et al. Characterization of Klebsiella sp. strain 10982, a colonizer of humans that contains novel antibiotic resistance alleles and exhibits genetic similarities to plant and clinical Klebsiella isolates. Antimicrob Agents Chemother 2014;58(4):1879-1888. https://doi.org/10.1128/AAC.01605-13
https://doi.org/10.1128/AAC.01605-13... ^,1010. Alves MS, Dias RC, de Castro AC, Riley LW, Moreira BM. Identification of clinical isolates of indole-positive and indole-negative Klebsiella spp. J Clin Microbiol 2006;44(10):3640-3646. https://doi.org/10.1128/JCM.00940-06
https://doi.org/10.1128/JCM.00940-06... ^,1111. van Veen SQ, Claas EC, Kuijper EJ. High-throughput identification of bacteria and yeast by matrix-assisted laser desorption ionization-time of flight mass spectrometry in conventional medical microbiology laboratories. J Clin Microbiol 2010;48(3):900-907. https://doi.org/10.1128/JCM.02071-09
https://doi.org/10.1128/JCM.02071-09... The phylogenetic analysis of the rpoB gene is more adequate than the 16S rRNA for Klebsiella spp. differentiation.¹²12. Martinez J, Martinez L, Rosenblueth M, Silva J, Martinez-Romero E. How are gene sequence analyses modifying bacterial taxonomy? The case of Klebsiella. Int Microbiol 2004;7(4):261-268. Likewise, K. variicola DX120E was identified both by 16S rRNA as rpoB genes, however, a better resolution was obtained with rpoB gene analysis.¹³13. Chun-Yan W, Li L, Li-Jing L, Yong-Xiu X, Chun-Jin H, Li-Tao Y, et al. Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol Fertil Soils 2014;50(4):657-666. https://doi.org/10.1007/s00374-013-0878-3
https://doi.org/10.1007/s00374-013-0878-... In addition, K. variicola described in animals and plants was also included in the rpoB phylogenetic analysis.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... Previously concatenated housekeeping genes were proposed to differentiate of Klebsiella species.¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... ^,33. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... With this criterium K. pneumoniae 342 from maize,¹⁴14. Fouts DE, Tyler HL, DeBoy RT, Daugherty S, Ren Q, Badger JH, et al. Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 2008;4(7):e1000141. https://doi.org/10.1371/journal.pgen.1000141
https://doi.org/10.1371/journal.pgen.100... and K. pneumoniae KP5-1 from insect¹⁵15. Medrano EG, Forray MM, Bell AA. Complete genome sequence of a Klebsiella pneumoniae strain isolated from a known cotton insect boll vector. Genome Announc 2014;2(4):pii: e00850-14. https://doi.org/10.1128/genomeA.00850-14
https://doi.org/10.1128/genomeA.00850-14... were found to be misclassified as K. pneumoniae.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... Actually the new K. variicola and K. pneumoniae isolates may now be properly identified by PCR. The first multiplex PCR, M-PCR-1 based on unique genes from each species would allow the differentiation in clinical laboratories of K. variicola and K. pneumoniae bacterial species.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... In the present study, the nucleotide BLAST analyses of rpoB gene sequence allowed the analysis of 419 Klebsiella spp. Genomes. All those strains with rpoB genes with 100% nucleotide identity to rpoB of K. pneumoniae MGH78578 were not further considered, as they had a correct taxonomic affiliation. 144 non-redundant DNA sequences were used for a phylogenetic analysis, showing seventeen putative K. pneumoniae strains corresponding to K. variicola bacterial species (figure 1). Their reported identification was K. pneumoniae MGH20, MGH40, MGH68, MGH76, MGH80, MGH92, MGH114, UCI18, BIDMC61, BIDMC88, BIDMC90, 223/14, KTE92, UCICRE10, B1, and CH4 and Klebsiella spp. 1.1.55. The Klebsiella spp. 1.1.55 clinical isolate was previously identified as a possible K. variicola.⁴4. Hazen TH, Zhao L, Sahl JW, Robinson G, Harris AD, Rasko DA, et al. Characterization of Klebsiella sp. strain 10982, a colonizer of humans that contains novel antibiotic resistance alleles and exhibits genetic similarities to plant and clinical Klebsiella isolates. Antimicrob Agents Chemother 2014;58(4):1879-1888. https://doi.org/10.1128/AAC.01605-13
https://doi.org/10.1128/AAC.01605-13... In addition, K. pneumoniae UCICRE14 corresponded to K. quasipneumoniae subsp. quasipneumoniae (KpII-A), whereas the K. pneumoniae 12-3578, ATCC 700603, MGH44 and HKUOPLC and K. variicola HKUOPLA corresponded to K. quasipneumoniae subsp. similipneumoniae (KpII-B) (figure 1).

Validation by average nucleotide identity analysis

The results obtained by phylogenetic analysis of rpoB gene were confirmed by determining the ANI value (table I). K. variicola At-22, K. quasipneumoniae 18A069, K. quasipneumoniae subsp. similipneumoniae 07A044 and K. pneumoniae MGH78578 were used as reference genomes in the ANI platform. This platform may use draft or complete genomes.⁷7. National Library of Medicine. Basic Local Alignment Search Tool (BLAST) [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information [cited 2016 Jan]. Available from: https://blast.ncbi.nlm.nih.gov/Blast.cgi
https://blast.ncbi.nlm.nih.gov/Blast.cgi... When strains from the same subspecies were compared, ANI was >99%. Among the K. variicola genomes, an ANI value of >99.08 was obtained; similarly, an ANI value of >99.15% for the K. quasipneumoniae genomes was obtained. For the K. pneumoniae and Klebsiella spp. genomes that were identified as K. variicola in the present study, ANI values were <94.01% compared with those of K. pneumoniae MGH-78578. In contrast, an ANI value of >98.89% was obtained when K. variicola isolates were compared to K. variicola At-22 (table I). Previously, Chen and colleagues ⁵5. Chen M, Li Y, Li S, Tang L, Zheng J, An Q. Genomic identification of nitrogen-fixing Klebsiella variicola, K. pneumoniae and K. quasipneumoniae. J Basic Microbiol 2016;56(1):78-84. https://doi.org/10.1002/jobm.201500415
https://doi.org/10.1002/jobm.201500415... detected nine misclassified K. variicola and four K. quasipneumoniae genomes. This update of Klebsiella genomes highlight that not only K. pneumoniae are misclassified, but also, K. variicola.

Not only K. pneumoniae and K. variicola but also K. quasipneumoniae isolates are not differentiated by biochemical methods. To address this problem, Brisse and colleagues¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... proposed a phylogenetic analysis based on five protein-coding genes (rpoB, fusA, gapA, gyrA, and leuS) that clearly differentiates K. variicola and K. quasipneumoniae from K. pneumoniae bacterial species. Nevertheless, we previously showed that the rpoB nucleotide partial gene sequence (501 bases) also supports the differentiation of K. variicola and K. pneumoniae.³3. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... This work confirms the correct taxonomic affiliation using the complete rpoB gene sequence.

General characteristics of K. variicola and K. quasipneumoniae strains and genomes

Misclassified K. pneumoniae and K. variicola genomes, now know to corresponded to K. variicola or K. quasipneumoniae, were submitted to GenBank in 2009. Other misclassified strains, such as Klebsiella spp. 1.1.55, and K. pneumoniae 342 genomes were deposited in 2008 (table II). The latter was reported to correspond to K. variicola in subsequent studies.¹1. Brisse S, Passet V, Grimont PA. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146-3152. https://doi.org/10.1099/ijs.0.062737-0
https://doi.org/10.1099/ijs.0.062737-0... ^,33. Garza-Ramos U, Silva-Sanchez J, Martinez-Romero E, Tinoco P, Pina-Gonzales M, Barrios H, et al. Development of a multiplex-PCR probe system for the proper identification of Klebsiella variicola. BMC Microbiol 2015;15:64. https://doi.org/10.1186/s12866-015-0396-6
https://doi.org/10.1186/s12866-015-0396-... ^,1616. Rosenblueth M, Martinez L, Silva J, Martinez-Romero E. Klebsiella variicola, a novel species with clinical and plant-associated isolates. Syst Appl Microbiol 2004;27(1):27-35. https://doi.org/10.1078/0723-2020-00261
https://doi.org/10.1078/0723-2020-00261... Genome submissions were mainly to USA, Mexico and Malaysia, with the USA as the major contributor (table II). These isolates were obtained from many different sources, such as humans (from urine, pus bile and other organic tisues), giant pandas (feces), different sites of plants, and from diverse insect species (table II). The majority of bacterial genomes were submitted as drafts with 12 to 400 contigs, using mostly Illumina technology. Five K. variicola genomes were completely sequenced using the Sanger shotgun, PacBio and 454 technologies (completed by Sanger sequencing of gaps), and the draft genomes contained from 24 to 464 contigs.

The K. quasipneumoniae genomes were submitted in 2013 and 2015 from different countries, including Austria, China, Germany, Spain and USA. All of these genomes were isolated from humans and were sequenced using the Illumina platform, with contigs from 1 to 476 and genome sizes >5 Mb and a content of CDS or proteins of 4 757 to 5 287 (table II).

Final considerations

It is a fact that Klebsiella spp. isolates have been misclassified. Several isolates of both K. variicola and K. quasipneumoniae from various sources were identified as K. pneumoniae. We report here, on a genomic basis, on misclassified K. pneumoniae, K. quasipneumoniae and K. variicola isolates from humans, animals, plants and insects. Nevertheless, the recent use of different methods such as PCR, phylogenetic analysis of rpoB gene and ANI for the proper differentiation of K. variicola and K. quasipneumoniae from K. pneumoniae will help the adequate classification of Klebsiella species. This work contributes to recognizing the extensive presence of K. variicola and K. quasipneumoniae in diverse sites and samples. The correct identification of K. variicola in the hospital setting could contribute to a more appropriate medical treatment.¹⁷17. Maatallah M, Vading M, Kabir MH, Bakhrouf A, Kalin M, Naucler P, et al. Klebsiella variicola is a frequent cause of bloodstream infection in the stockholm area, and associated with higher mortality compared to K. pneumoniae. PloS One 2014;9(11):e113539. https://doi.org/10.1371/journal.pone.0113539
https://doi.org/10.1371/journal.pone.011... Notably, some K. variicola¹⁸18. Di DY, Jang J,Unno T, Hur HG. Emergence of Klebsiella variicola positive for NDM-9, a variant of New Delhi metallo-β-lactamase, in an urban river in South Korea. J Antimicrob Chemother 2017;72(4):1063-1067. https://doi.org/10.1093/jac/dkw547
https://doi.org/10.1093/jac/dkw547... ^,1919. Hopkins KL, Findlay J, Doumith M, Mather B, Meunier D, D’Arcy S, et al. IMI-2 carbapenemase in a clinical Klebsiella variicola isolated in the UK. J Antimicrob Chemother 2017;72(7):2129-2131. https://doi.org/10.1093/jac/dkx103
https://doi.org/10.1093/jac/dkx103... and K. quasipneumoniae,²⁰20. Breurec S, Melot B, Hoen B, Passet V, Schepers K, Bastian S, et al. Liver Abscess Caused by Infection with Community-Acquired Klebsiella quasipneumoniae subsp. quasipneumoniae. Emerg Infect Dis 2016;22(3):529-531. https://doi.org/10.3201/eid2203.151466
https://doi.org/10.3201/eid2203.151466... respectively, have acquired carbapenem resistance and virulence factors.

Acknowledgments

This work was supported by grant CB-2015-01-256988 from SEP-Conacyt (Secretaría de Educación Pública-Consejo Nacional de Ciencia y Tecnología) . We thank Angelina Quiterio for her excellent laboratory assistance and Michael Dunn and J. Martinez-Romero for their help in reviewing the manuscript. EP-R was supported by a grant (IN-201117) from PAPIIT-DGAPA, UNAM.

Referencias

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