Diversity, functional classification and genotyping of SHV β-lactamases in Klebsiella pneumoniae Article Swipe

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Kara K. Tsang , Margaret M. C. Lam , Ryan R. Wick , Kelly L. Wyres , Michael A. Bachman , Stephen Baker , Katherine Barry , Sylvain Brisse , Susana Campino , Alexandra Chiaverini , Daniela María Cirillo , Taane G. Clark , Jukka Corander , Marta Corbella , Alessandra Cornacchia , Aline Cuénod , Nicola D’Alterio , Federico Di Marco , Pilar Donado-Godoy , Adrian Egli , Refath Farzana , Edward J. Feil , Aasmund Fostervold , Claire L. Gorrie , Brekhna Hassan , Marit Andrea Klokkhammer Hetland , Le Nguyen Minh Hoa , Le Thi Hoi , Benjamin P. Howden , Odion O. Ikhimiukor , Adam Jenney , Håkon Kaspersen , Fahad Khokhar , Thongpan Leangapichart , Małgorzata Ligowska-Marzęta , Iren H. Löhr , S. Wesley Long , Amy J. Mathers , Andrew G. McArthur , Geetha Nagaraj , Anderson O. Oaikhena , Iruka N. Okeke , João Perdigão , Hardik I. Parikh , My H. Pham , Francesco Pomilio , Niclas Raffelsberger , Andriniaina Rakotondrasoa , K. L. Ravi Kumar , Leah W. Roberts , Carla Rodrigues , Ørjan Samuelsen , Kirsty Sands , Davide Sassera , Helena M. B. Seth-Smith , Varun Shamanna , Norelle L. Sherry , Sonia Sia , Anton Spadar , Nicole Stoesser , Marianne Sunde , Arnfinn Sundsfjord , Phạm Ngọc Thạch , Nicholas R. Thomson , Harry A. Thorpe , M. Estée Török , Van Dinh Trang , Nguyen Vu Trung , Jay Vornhagen , Timothy R. Walsh , Ben Warne , Hayley Wilson , Gerard D. Wright , Kathryn E. Holt ·

YOU? · · 2024 · Open Access · · DOI: https://doi.org/10.1099/mgen.0.001294

Interpreting the phenotypes of bla SHV alleles in Klebsiella pneumoniae genomes is complex. Whilst all strains are expected to carry a chromosomal copy conferring resistance to ampicillin, they may also carry mutations in chromosomal bla SHV alleles or additional plasmid-borne bla SHV alleles that have extended-spectrum β-lactamase (ESBL) activity and/or β-lactamase inhibitor (BLI) resistance activity. In addition, the role of individual mutations/a changes is not completely documented or understood. This has led to confusion in the literature and in antimicrobial resistance (AMR) gene databases [e.g. the National Center for Biotechnology Information (NCBI) Reference Gene Catalog and the β-lactamase database (BLDB)] over the specific functionality of individual sulfhydryl variable (SHV) protein variants. Therefore, the identification of ESBL-producing strains from K. pneumoniae genome data is complicated. Here, we reviewed the experimental evidence for the expansion of SHV enzyme function associated with specific aa substitutions. We then systematically assigned SHV alleles to functional classes (WT, ESBL and BLI resistant) based on the presence of these mutations. This resulted in the re-classification of 37 SHV alleles compared with the current assignments in the NCBI’s Reference Gene Catalog and/or BLDB (21 to WT, 12 to ESBL and 4 to BLI resistant). Phylogenetic and comparative genomic analyses support that (i) SHV-1 (encoded by bla SHV-1 ) is the ancestral chromosomal variant, (ii) ESBL- and BLI-resistant variants have evolved multiple times through parallel substitution mutations, (iii) ESBL variants are mostly mobilized to plasmids and (iv) BLI-resistant variants mostly result from mutations in chromosomal bla SHV . We used matched genome–phenotype data from the KlebNET-GSP AMR Genotype-Phenotype Group to identify 3999 K . pneumoniae isolates carrying one or more bla SHV alleles but no other acquired β-lactamases to assess genotype–phenotype relationships for bla SHV . This collection includes human, animal and environmental isolates collected between 2001 and 2021 from 24 countries. Our analysis supports that mutations at Ambler sites 238 and 179 confer ESBL activity, whilst most omega-loop substitutions do not. Our data also provide support for the WT assignment of 67 protein variants, including 8 that were noted in public databases as ESBL. These eight variants were reclassified as WT because they lack ESBL-associated mutations, and our phenotype data support susceptibility to third-generation cephalosporins (SHV-27, SHV-38, SHV-40, SHV-41, SHV-42, SHV-65, SHV-164 and SHV-187). The approach and results outlined here have been implemented in Kleborate v2.4.1 (a software tool for genotyping K. pneumoniae ), whereby known and novel bla SHV alleles are classified based on causative mutations. Kleborate v2.4.1 was updated to include ten novel protein variants from the KlebNET-GSP dataset and all alleles in public databases as of November 2023. This study demonstrates the power of sharing AMR phenotypes alongside genome data to improve the understanding of resistance mechanisms.

Related Topics

Biology

Klebsiella Pneumoniae

Phylogenetic Tree

Escherichia Coli

Concepts

Biology Klebsiella pneumoniae Genetics Gene Genotyping Plasmid Genome Allele Phylogenetic tree Genotype Escherichia coli

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Type: review
Language: en
Landing Page: https://doi.org/10.1099/mgen.0.001294
OA Status: gold
Cited By: 12
References: 57
Related Works: 10
OpenAlex ID: https://openalex.org/W4403601020

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OpenAlex ID: https://openalex.org/W4403601020

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DOI: https://doi.org/10.1099/mgen.0.001294

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Title: Diversity, functional classification and genotyping of SHV β-lactamases in Klebsiella pneumoniae

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Type: review

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Language: en

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Publication year: 2024

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Publication date: 2024-10-21

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Authors: Kara K. Tsang, Margaret M. C. Lam, Ryan R. Wick, Kelly L. Wyres, Michael A. Bachman, Stephen Baker, Katherine Barry, Sylvain Brisse, Susana Campino, Alexandra Chiaverini, Daniela María Cirillo, Taane G. Clark, Jukka Corander, Marta Corbella, Alessandra Cornacchia, Aline Cuénod, Nicola D’Alterio, Federico Di Marco, Pilar Donado-Godoy, Adrian Egli, Refath Farzana, Edward J. Feil, Aasmund Fostervold, Claire L. Gorrie, Brekhna Hassan, Marit Andrea Klokkhammer Hetland, Le Nguyen Minh Hoa, Le Thi Hoi, Benjamin P. Howden, Odion O. Ikhimiukor, Adam Jenney, Håkon Kaspersen, Fahad Khokhar, Thongpan Leangapichart, Małgorzata Ligowska-Marzęta, Iren H. Löhr, S. Wesley Long, Amy J. Mathers, Andrew G. McArthur, Geetha Nagaraj, Anderson O. Oaikhena, Iruka N. Okeke, João Perdigão, Hardik I. Parikh, My H. Pham, Francesco Pomilio, Niclas Raffelsberger, Andriniaina Rakotondrasoa, K. L. Ravi Kumar, Leah W. Roberts, Carla Rodrigues, Ørjan Samuelsen, Kirsty Sands, Davide Sassera, Helena M. B. Seth-Smith, Varun Shamanna, Norelle L. Sherry, Sonia Sia, Anton Spadar, Nicole Stoesser, Marianne Sunde, Arnfinn Sundsfjord, Phạm Ngọc Thạch, Nicholas R. Thomson, Harry A. Thorpe, M. Estée Török, Van Dinh Trang, Nguyen Vu Trung, Jay Vornhagen, Timothy R. Walsh, Ben Warne, Hayley Wilson, Gerard D. Wright, Kathryn E. Holt

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Landing page: https://doi.org/10.1099/mgen.0.001294

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OA URL: https://doi.org/10.1099/mgen.0.001294

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Concepts: Biology, Klebsiella pneumoniae, Genetics, Gene, Genotyping, Plasmid, Genome, Allele, Phylogenetic tree, Genotype, Escherichia coli

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Cited by: 12

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abstract_inverted_index.we	125
abstract_inverted_index.(21	185
abstract_inverted_index.(i)	203
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abstract_inverted_index.AMR	257, 440
abstract_inverted_index.BLI	154, 194
abstract_inverted_index.Our	303, 323
abstract_inverted_index.SHV	5, 35, 41, 134, 146, 170, 247, 272, 285, 401
abstract_inverted_index.The	376
abstract_inverted_index.WT,	187
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abstract_inverted_index.bla	4, 34, 40, 207, 246, 271, 284, 400
abstract_inverted_index.but	274
abstract_inverted_index.for	88, 130, 283, 328, 391
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abstract_inverted_index.led	71
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abstract_inverted_index.one	268
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abstract_inverted_index.ten	415
abstract_inverted_index.the	1, 57, 75, 85, 96, 101, 112, 127, 131, 158, 166, 174, 178, 211, 255, 329, 420, 436, 447
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abstract_inverted_index.(WT,	151
abstract_inverted_index.(ii)	215
abstract_inverted_index.(iv)	237
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abstract_inverted_index.2021	299
abstract_inverted_index.3999	262
abstract_inverted_index.BLDB	184
abstract_inverted_index.ESBL	152, 190, 229, 315
abstract_inverted_index.Gene	93, 181
abstract_inverted_index.This	69, 163, 287, 433
abstract_inverted_index.also	29, 325
abstract_inverted_index.been	383
abstract_inverted_index.copy	22
abstract_inverted_index.data	121, 253, 324, 361, 444
abstract_inverted_index.from	117, 242, 254, 300, 419
abstract_inverted_index.gene	82
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abstract_inverted_index.not.	322
abstract_inverted_index.over	100
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abstract_inverted_index.that	43, 202, 306, 338
abstract_inverted_index.then	143
abstract_inverted_index.they	27, 354
abstract_inverted_index.tool	390
abstract_inverted_index.used	250
abstract_inverted_index.were	339, 349
abstract_inverted_index.with	138, 173
abstract_inverted_index.(AMR)	81
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abstract_inverted_index.(SHV)	108
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abstract_inverted_index.2023.	432
abstract_inverted_index.ESBL-	216
abstract_inverted_index.ESBL.	345
abstract_inverted_index.Group	259
abstract_inverted_index.Here,	124
abstract_inverted_index.SHV-1	204, 208
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abstract_inverted_index.based	156, 405
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abstract_inverted_index.(NCBI)	91
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abstract_inverted_index.genome	120, 443
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abstract_inverted_index.v2.4.1	387, 410
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abstract_inverted_index.(BLDB)]	99
abstract_inverted_index.Catalog	94, 182
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abstract_inverted_index.SHV-38,	368
abstract_inverted_index.SHV-40,	369
abstract_inverted_index.SHV-41,	370
abstract_inverted_index.SHV-42,	371
abstract_inverted_index.SHV-65,	372
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abstract_inverted_index.National	86
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abstract_inverted_index.analysis	304
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abstract_inverted_index.parallel	225
abstract_inverted_index.plasmids	235
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abstract_inverted_index.variant,	214
abstract_inverted_index.variants	219, 230, 239, 348, 418
abstract_inverted_index.Kleborate	386, 409
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abstract_inverted_index.SHV-187).	375
abstract_inverted_index.activity,	316
abstract_inverted_index.activity.	54
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abstract_inverted_index.ancestral	212
abstract_inverted_index.causative	407
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abstract_inverted_index.confusion	73
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abstract_inverted_index.including	336
abstract_inverted_index.inhibitor	51
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abstract_inverted_index.variants,	335
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abstract_inverted_index.Klebsiella	8
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abstract_inverted_index.mutations,	227, 357
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abstract_inverted_index.pneumoniae	9, 119, 265, 394
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abstract_inverted_index.sulfhydryl	106
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abstract_inverted_index.KlebNET-GSP	256, 421
abstract_inverted_index.ampicillin,	26
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abstract_inverted_index.implemented	384
abstract_inverted_index.mechanisms.	451
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abstract_inverted_index.resistant).	195
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abstract_inverted_index.substitution	226
abstract_inverted_index.β-lactamase	46, 50, 97
abstract_inverted_index.BLI-resistant	218, 238
abstract_inverted_index.Biotechnology	89
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abstract_inverted_index.identification	113
abstract_inverted_index.substitutions.	141
abstract_inverted_index.susceptibility	363
abstract_inverted_index.systematically	144
abstract_inverted_index.ESBL-associated	356
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abstract_inverted_index.extended-spectrum	45
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countries_distinct_count	16
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