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Identification of a Recently Dominate Sublineage in Salmonella 4,[5],12:I

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Identification of a Recently Dominate Sublineage in Salmonella 4,[5],12:I bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 RESEARCH 2 3 Identification of a recently dominate sublineage in Salmonella 4,[5],12:i:- 4 sequence type 34 isolated from food animals in Japan 5 6 Running head 7 Recent spread of Salmonella 4,[5],12:i:- in Japan 8 9 Nobuo Arai, Tsuyoshi Sekizuka, Yukino Tamamura-Andoh, Lisa Barco, Atsushi Hinenoya, Shinji 10 Yamasaki, Taketoshi Iwata, Ayako Watanabe-Yanai, Makoto Kuroda, Masato Akiba, and Masahiro 11 Kusumoto 12 13 Author affiliations: National Institute of Animal Health, National Agriculture and Food Research 14 Organization, Ibaraki, Japan (N. Arai, Y. Tamamura-Andoh, T. Iwata, A. Watanabe-Yanai, M. 15 Akiba, M. Kusumoto); Osaka Prefecture University, Osaka, Japan (N. Arai, A. Hinenoya, S. 16 Yamasaki, M. Akiba); National Institute of Infectious Diseases, Tokyo, Japan (T. Sekizuka, M. 17 Kuroda); Istituto Zooprofilattico Sperimentale delle Venezie, Padova, Italy (L. Barco) 18 19 Address for correspondence: Masahiro Kusumoto, National Institute of Animal Health, National 20 Agriculture and Food Research Organization, 3-1-5 Kannondai, Tsukuba, Ibaraki 305-0856, Japan; 21 email, [email protected]; phone/fax, +81-29-838-7749. 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 22 Abstract 23 Salmonella Typhimurium and its monophasic variant (Salmonella 4,[5],12:i:-) are classified 24 into nine clades. Clade 9 is composed of ST34 strains, including the Salmonella 4,[5],12:i:- 25 European clone, which has rapidly disseminated in humans and animals worldwide since the 2000s. 26 To reveal the microevolution of ST34/clade 9, we analyzed the whole-genome-based phylogenetic 27 relationships of 230 Salmonella Typhimurium and Salmonella 4,[5],12:i:- strains isolated between 28 1998 and 2017 in Japan and other countries. We identified clade 9-2, a novel sublineage derived 29 from the conventional Salmonella 4,[5],12:i:- clade 9 that exclusively consists of Japanese isolates. 30 Clade 9-2 was generated by mobile genetic element-mediated stepwise genome reductions caused 31 by IS26 and prophages. Furthermore, the recently identified strains developed further resistance 32 to antimicrobials via the acquisition of resistance genes. During this microevolution, Salmonella 33 4,[5],12:i:- clade 9-2 has dominated among recent isolates from food animals in Japan via the 34 emergence of clonally expanding and/or multiple host-adapted subclades. 35 (149/150 words) 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 36 Introduction 37 Salmonella enterica subsp. enterica serovar Typhimurium and its monophasic variant 38 (Salmonella 4,[5],12:i:-) are two of the most common gastrointestinal pathogens for both humans 39 and animals worldwide (1, 2). Salmonella 4,[5],12:i:- infections have been increasingly occurring 40 in European countries since the 2000s and have since spread to the United States, South America, 41 Australia, and Asia (3-9). A European clone is one of the best studied Salmonella 4,[5],12:i:- 42 isolates because of its rapid and worldwide dissemination (6, 9-11). Swine was reported as the 43 main reservoir of this clone, and the contaminated products are considered causative agents of 44 food-borne infection (12). The European clone is characterized by sequence type (ST) 34 and 45 possession of two mobile genetic elements (MGEs) on the chromosome: a composite transposon, 46 which is responsible for resistance to core antimicrobials including ampicillin, streptomycin, 47 sulfonamides, and tetracycline (R-type ASSuT), and an 81-kb integrative and conjugative element 48 (ICE) containing heavy-metal tolerance genes (10). The ST34-specific ICE was first identified in 49 Salmonella 4,[5],12:i:- and was named Salmonella genomic island 3 (SGI-3) in 2016 (10). 50 However, Moreno Switt et al. identified nine genomic islands in several Salmonella serovars and 51 designated them as SGI-2 to SGI-10 (13). Therefore, we propose to redesignate the ST34-specific 52 ICE as ICEmST in the present study because the SGI number-based discrimination of Salmonella 53 ICE is confusing. 54 In Japan, cases of cattle and swine salmonellosis caused by Salmonella 4,[5],12:i:- have 55 increased over the past decade (14, 15). We previously classified 119 Salmonella 56 Typhimurium/4,[5],12:i:- strains isolated in Japan and Italy into nine clades by whole-genome- 57 based phylogenetic analysis (16). Among the nine clades, clade 9 was composed of Salmonella 58 Typhimurium/4,[5],12:i:- and regarded as the European clone. We also developed a PCR-based 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 59 clade typing method and classified another 955 Salmonella Typhimurium/4,[5],12:i:- strains 60 isolated from animals in Japan (16). Clade 9 was the most predominant among the 955 strains and 61 consisted of 210 strains: two Salmonella Typhimurium strains isolated in 1998 and 208 Salmonella 62 4,[5],12:i:- strains isolated between 2002 and 2017. Clade 9 strains were found in the 1990s and 63 early 2000s but have dominated since approximately 2012; thus, the rapid dissemination of clade 64 9 strains in Japan may have occurred in the mid-2000s or later. 65 A major factor underlying the generation of the monophasic variant of Salmonella 66 Typhimurium was the absence of fljB encoding the phase 2-H antigen (14). Other causes were the 67 following amino acid substitutions in proteins that induced phase variation: A46T in FljA and 68 R140L in Hin (14). In the Salmonella 4,[5],12:i:- European clone, the absence of fljB and the 69 flanking region resulted in the expression of only one H antigen (10, 17), but how fljB and the 70 flanking region were deleted from the European clone remains unclear. 71 The acquisition of resistance to clinically important antimicrobials is a well-studied factor 72 regarding the clonal expansion of bacterial strains (18). Several studies have reported the 73 acquisition of antimicrobial resistance (AMR) in addition to core antimicrobials in Salmonella 74 4,[5],12:i- ST34; the recent swine isolates acquired trimethoprim and/or gentamycin resistance via 75 plasmids in the United Kingdom (19), and human isolates possessed a large IncHI2 plasmid (246 76 kb) carrying multiple AMR genes in Vietnam (11). MGEs are known to play an important role in 77 the transmission of various genes, but the factors underlying the acquisition of such large plasmids 78 by recently isolated ST34 strains have not been fully elucidated. 79 In the present study, we investigated the phylogenetic relationships of 230 Salmonella 80 Typhimurium/4,[5],12:i:- clade 9 strains isolated from food animals in Japan and some other 81 countries and analyzed the microevolution focusing on the generation of the monophasic variant. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 82 We report the emergence of a novel sublineage in Salmonella 4,[5],12:i:- clade 9 that has 83 dominated in recent isolates from food animals in Japan. 84 85 Materials and Methods 86 A total of 227 Salmonella Typhimurium/4,[5],12:i:- strains isolated in Japan and Italy (214 87 and 13 strains, respectively) were used in this study (Technical Appendix Table 1), and all strains 88 have already been identified as belonging to ST34/clade 9 (16). Detailed information on the 89 Japanese strains is shown in Technical Appendix Table 2. Among the 227 strains, the whole- 90 genome sequences of 200 strains isolated in Japan were analyzed in this study, and those of the 91 remaining 27 strains were reported in our previous study (16). We selected the whole-genome 92 sequences of Salmonella 4,[5],12:i:- ST34, which are well supported by epidemiological 93 information, from the National Center for Biotechnology Information database and added the data 94 of the Australian strain TW-Stm6 and Chinese strains 81741 and WW012 (accession numbers 95 CP019649.1, CP019442.1, and CP022168.1, respectively) for phylogenetic analysis. 96 Extraction of single nucleotide polymorphisms (SNPs) from the core genomes of the 230 97 strains was performed according to the procedures described in the Technical Appendix. To 98 analyze the phylogenetic relationships, a maximum-likelihood (ML) tree was generated by using 99 RAxML (20). To reveal the divergence history, we performed a temporal phylogenetic analysis of 100 the SNPs of 214 Japanese strains by using BEAST (21) and estimated the years of emergence of 101 distinct clades. The population structure was analyzed by hierBAPS (22) using a Bayesian 102 clustering method. 103 AMR genes, plasmid replicon types, prophages, and ICEmST were identified in whole- 104 genome sequences by the methods described in the Technical Appendix. Comparison of the 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.14.338830; this version posted October 14, 2020.
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