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The Canadian Journal of Infectious Diseases & Medical Microbiology = Journal Canadien des Maladies Infectieuses et de la Microbiologie Médicale logoLink to The Canadian Journal of Infectious Diseases & Medical Microbiology = Journal Canadien des Maladies Infectieuses et de la Microbiologie Médicale
. 2020 Mar 30;2020:9205197. doi: 10.1155/2020/9205197

Comparative Genomics Reveals Pathogenicity-Related Loci in Shewanella algae

Jui-Hsing Wang 1,2, Guo-Cheng He 3, Yao-Ting Huang 2,✉, Po-Yu Liu 4,5,6,✉
PMCID: PMC7149415  PMID: 32318128

Abstract

Shewanella algae is an emerging marine zoonotic pathogen and accounts for considerable mortality and morbidity in compromised hosts. However, there is scarce literature related to the understanding of the genetic background of virulence determinants in S. algae. In this study, we aim to determine the occurrence of common virulence genes in S. algae using whole-genome sequence and comparative genomic analysis. Comparative genomics reveals putative-virulence genes related to bile resistance, chemotaxis, hemolysis, and motility. We detected the existence of hlyA, hlyD, and hlyIII involved in hemolysis. We also found chemotaxis gene cluster cheYZA operon and cheW gene. The results provide insights into the genetic basis underlying pathogenicity in S. algae.

1. Introduction

Shewanella algae is an emerging marine zoonotic pathogen. The organism was first classified in 1990 by Simidu et al. [1], emended by Nozue et al. [2], and described as a Gram-negative, motile bacillus, with hydrogen sulfide production, exhibiting hemolysis on sheep blood agar. S. algae is found in marine environments throughout the world and has been linked with both human and marine animal infections [3, 4]. Currently, there are at least three other Shewanella species found in clinical specimens and S. algae accounts for the majority of isolates from humans [5, 6]. S. algae has also been reported to cause diseases in marine animal, both wild and cultured [7–9]. However, there is scarce literature related to the understanding of the genetic background of virulence determinants in S. algae.

Marine ecosystem consists of a large variety of organisms that impact human health [10]. The advance of sequencing technology allows the identification of determinants in pathogenic microorganisms and has become an important approach to study the fundamental mechanisms of pathogenesis [11, 12]. Comparative genomics further enables the investigation of core elements of pathogenesis factors in great detail [13]. Recently, there have been attempts to use whole-genome sequencing in the study of marine pathogens [14]. Therefore, genomic comparison of the clinical S. algae isolates could provide clues for pathogenic or fitness determinants [15].

The aims of the study were to determine the occurrence of common virulence genes found in S. algae isolates from clinical setting using whole-genome sequence and comparative genomic analysis and to explore the relationship among the tested genomes.

2. Materials and Methods

2.1. Bacterial Strains, Media, and Growth Conditions

S. algae strains ACCC, YHL, and CHL were obtained from various clinical sources (Table 1). Glycerol stock of stored isolates was grown in trypticase soy agar with 5% sheep blood (Becton, Dickinson and Company, Franklin Lakes, NJ, USA) at 30°C for 24 hours. Single colonies were inoculated in tryptic soy broth (Becton, Dickinson and Company, Franklin Lakes, NJ). The isolates were preliminarily identified using 16S rRNA gene sequencing and matrix-assisted laser desorption ionization-time of flight mass spectrometry (bioMérieux, Marcy l'Etoile, France). A part of 16S rRNA gene was amplified using the primers of B27F (5′-AGAGTTTGATCCTGGCTCAG-3′) and U1492R (5′-GGTTACCTTGTTACGACTT-3′) [9, 16]. The nucleotide sequences were aligned, and BLAST search was performed against the GenBank database of the National Center for Biotechnology Information (NCBI) [17].

Table 1.

Strains and genomic features of S. algae strains in this study.

Strain Isolation source Geographic origin Genome assembly status Genome coverage Genome size (bp) GC content (%) CDSs Pseudogenes rRNA operons tRNAs
CHL Bile Taiwan Scaffold 243.0x 4,888,589 52.96 4,281 122 6, 5, 2 (5S, 16S, 23S) 88
YHL Wound Taiwan Scaffold 257.0x 4,850,439 53.00 4,212 71 6, 5, 2 (5S, 16S, 23S) 86
ACCC Bile Taiwan Scaffold 186.0x 4,744,804 53.08 4,223 143 4, 4 (5S, 16S) 91
MARS 14 Lung France Scaffold 91.0x 5,005,849 52.90 4,347 90 6, 3, 3 (5S, 16S, 23S) 104
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2.2. Genome Sequencing and Assembly

Nucleic acids were extracted from overnight culture using the QIAGEN Genomic-tip 100/G kit and the Genomic DNA Buffer Set (QIAGEN, Paisley, UK) according to the manufacturer's protocol. The DNA concentrations were measured by Qubit dsDNA HS Assay kit using Qubit 2.0 fluorometer (Life Technologies, Carlsbad, CA, USA). The DNA sample was sheared, in a microTUBE using Covaris S2 (Covaris, Woburn, MA, USA), into the desired size fragment of the library. The indexed PCR-free library preparation was performed using multiplexed high-throughput sequencing TruSeq DNA Sample Preparation Kit (Illumina) with 2 μg of DNA on the basis of the manufacturer's introduction. Genome sequencing was performed using paired-end 250 bp sequencing on the Illumina MiSeq platform (Illumina, Inc., San Diego, CA). Raw sequence files were artifact-filtered and trimmed with DUK (http://duk.sourceforge.net/) and FASTX-toolkit fastx_trimmer (https://github.com/agordon/fastx_toolkit), respectively. Assembly was performed with a hybrid approach by ALLPATHS, version R46652 and Velvet version 1.2.07.

2.3. Public Genome Download

Genome sequence of human isolated S. algae MARS 14 was retrieved from the NCBI Genome website (https://www.ncbi.nlm.nih.gov/assembly/GCF_000947195.1/).

2.4. Phylogenetic Analysis Based on Whole-Genome Sequences

Genome-based phylogenic analysis was performed using pairwise comparison of average nucleotide identity. The whole-genome average nucleotide identity (ANI) was calculated with the use of a modified algorithm [18]. Phylogenetic trees were visualized using MEGA7.

2.5. Annotation and Comparative Genomics

The annotation was performed using the NCBI Prokaryotic Genome Annotation Pipeline (PGAP) [19] and the DOE-JGI Microbial Genome Annotation Pipeline version 4.10.5 [20]. The prediction was done using Glimmer 3.02 [21]. The nontranslated genes were predicted by tRNAscan-SE [22], RNAmmer [23], and RFAM [24]. Functional classification of the predicted genes was carried out using RPSBLAST program v. 2.2.15 [25]. Analysis of the functional annotation was further performed using the Integrated Microbial Genomes & Microbiomes system v.5.0 [26] and the Pathosystems Resource Integration Center [27]. CDS count for these strains was derived. Comparative genome analysis was performed using EDGAR platform (http://edgar.computational.bio) [28]. The core genome and the singletons for the 4 related S. algae genomes were generated for Prokka-annotated genomes using EDGAR (http://edgar.computational.bio). We compared the S. algae genomes using the MUMmer software package [29] together with the Circos visualization engine [30].

3. Results

3.1. Genome Sequencing and Assembly

The genomic sequencing consisted of 250 bp paired-end reads, yielding approximately 0.88 Gbp to 1.24 Gbp for each isolate. The de novo assembly of genome sequence data revealed that the number of contigs (>200 bp) varied from 27 to 74 for each genome. The maximum contig size among the genomes was 976,090 bp aligned to YHL. The GC content ranged from 52.96% for CHL to 53.08% for ACCC. Table 1 shows the descriptive statistics of the genomic characteristics for the strains in this study. The sequence data were publicly available in NCBI SRA database (accession number: ACCC [LVCY00000000.1], CHL [LVDF00000000.1], and YHL [LVDU00000000.1]).

3.2. Genome-Based Phylogenetic Analysis

The average nucleotide identity (ANI) was calculated and revealed that tested S. algae strains were identical in terms of nucleotide sequences, as shown in Figure 1.

Figure 1.

Figure 1

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Whole-genome phylogeny of S. algae in the study.

3.3. Comparative Genomics

We constructed a pan-genome dataset using whole-genome sequence of sequenced S. algae strains. Figure 2 shows orthologous genes shared among strains and depicts the position and color-coded function of the S. algae genes. The numbers of orthologous and strain-specific unique genes are shown in the Venn diagram. Core genome for the S. algae strains consists of 1354 coding sequences (Figure 3). The set of unique genes harbored by each strain varies from 335 for S. algae YHL to 466 for S. algae CHL. Following genome map construction, we conducted genome mapping among the S. algae strains in the study. In this comparison, colored arcs indicate regions of high similarity as revealed by the NUCmer script from the MUMmer software package. As shown in Figure 4, the alignment revealed an obvious syntenic relationship in these strains.

Figure 2.

Figure 2

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Circular genomes representation map and genome comparison of Shewanella algae (CHL, ACCC, MARS 14, and YHL). Predicted coding sequences (CDSs) are assigned various colors with respect to cellular functions. Circles show, from the outermost to the innermost, (1) DNA coordinates; (2, 3) function-based color-coded mapping of the CDSs predicted on the forward and reverse strands of the S. algae CHL genome, respectively; (4) orthologous CDSs shared between S. algae CHL and S. algae ACCC; (5) S. algae CHL-specific CDSs, compared with S. algae ACCC; (6) orthologous CDSs shared between S. algae CHL and S. algae MARS 14; (7) S. algae CHL-specific CDSs, compared with S. algae MARS 14; (8) orthologous CDSs shared between S. algae CHL and S. algae YHL; (9) S. algae CHL-specific CDSs, compared with S. algae YHL; (10) GC plot with regions above and below average in green and violet; (11) GC skew showing regions above and below average in yellow and light blue. This figure was plotted in Scalable Vector Graphics format via an in-house script, which calculates the radius and ribbon width according to the BLAST alignments and adds colors by COG classification of all orthogonal genes.

Figure 3.

Figure 3

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Comparison of the gene contents of the Shewanella algae in this study, Venn diagram showing the numbers of conserved and strain-specific coding sequences (CDSs).

Figure 4.

Figure 4

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Genomes mapping between strains in the study. Each colored arc indicates an orthologous match between two species. The color segments in the outer circle are randomly displayed and do not correspond to a particular scheme. A minimum seed match size of 500 bp was used.

3.4. Analysis of Putative-Virulence-Related Genes

As illustrated in Table 2, genes encoded exbBD, galU, and htpB are shared with S. algae genomes. Heat shock protein gene clpP and hemolysis homologous genes, hlyA, hlyD, hlyIII, and tolC, were found in each S. algae genome. Gene cluster cheYZA operon and cheW involved in chemotaxis were detected in all tested S. algae. Flagellar gene operons are present in all tested S. algae genome.

Table 2.

Virulence genes shared with S. algae strains in this study.

Gene locus_tag Length locus_tag Length locus_tag Length locus_tag Length
Strains MARS 14 YHL CHL ACCC
hlyA BN1227_RS19795 443 AYI97_RS17645 443 AYI82_RS07480 443 AYI77_RS13890 443
hlyD BN1227_RS18765 352 AYI97_RS03440 352 AYI82_RS00925 352 AYI77_RS05040 352
BN1227_RS19395 349 AYI97_RS04065 349 AYI82_RS01570 349 AYI77_RS08410 349
BN1227_RS08585 314 AYI97_RS05045 314 AYI82_RS17560 314 AYI77_RS14620 314
hlyIII BN1227_RS10295 226 AYI97_RS09385 226 AYI82_RS06545 226 AYI77_RS04320 226
tolC BN1227_RS02290 424 AYI97_RS03690
AYI97_RS12455
AYI97_RS17535
AYI97_RS18425		 466
438
467
491		 AYI82_RS01185
AYI82_RS03510
AYI82_RS07370		 466
438
467		 AYI77_RS01075
AYI77_RS01845
AYI77_RS02720
AYI77_RS04785
AYI77_RS13995		 491
BN1227_RS02895 438 438
BN1227_RS03705 491 424
BN1227_RS12395 438 466
BN1227_RS19025 466 467
BN1227_RS19685 467  
htpB (groL) BN1227_RS18535 546 AYI97_RS03170 546 AYI82_RS00700 546 AYI77_RS05265 546
galU BN1227_RS14240 303 AYI97_RS19990 303 AYI82_RS13425 303 AYI77_RS03360 303
AYI82_RS18495 294 AYI77_RS16730 294
exbB BN1227_RS13275 175 AYI97_RS02650 238 AYI82_RS00200 238 AYI77_RS07050 175
BN1227_RS13280 451 AYI97_RS04225 164 AYI82_RS01760 164 AYI77_RS07055 451
BN1227_RS17925 238 AYI97_RS14790 175 AYI82_RS21410 175 AYI77_RS08255 164
BN1227_RS19555 164 AYI97_RS14795 451 AYI82_RS21415 451 AYI77_RS08875 238
exbD BN1227_RS13270 134 AYI97_RS02655 135 AYI82_RS00205 135 AYI77_RS07045 134
BN1227_RS17930 135 AYI97_RS04230 135 AYI82_RS01765 135 AYI77_RS08250 135
BN1227_RS19560 135 AYI97_RS14785 134 AYI82_RS21405 134 AYI77_RS08870 135
cheY BN1227_RS07095 127 AYI97_RS06385 127 AYI82_RS05630 127 AYI77_RS20450 127
cheZ BN1227_RS07100 245 AYI97_RS06380 245 AYI82_RS05625 245 AYI77_RS20455 245
cheA BN1227_RS01115 701 AYI97_RS06375 776 AYI82_RS05620 770 AYI77_RS12010 696
BN1227_RS07105 776 AYI97_RS16805 696 AYI82_RS09360 701 AYI77_RS20925 754
cheW BN1227_RS07130 164 AYI97_RS06350 164 AYI82_RS05595 164 AYI77_RS20950 164
BN1227_RS01120 183 AYI97_RS16800 183 AYI82_RS05600 336 AYI77_RS12015 183
BN1227_RS07125 336 AYI97_RS06355 335 AYI82_RS09355 183 AYI77_RS20945 336
clpP BN1227_RS08465 202 AYI97_RS05170 202 AYI82_RS17685 202 AYI77_RS14495 202
FlgA BN1227_RS06885 235 AYI97_RS06595 235 AYI82_RS05050 248 AYI77_RS09380 248
BN1227_RS21260 248 AYI97_RS14310 248 AYI82_RS05840 235 AYI77_RS20850 235
FlgB BN1227_RS06900 132 AYI97_RS06580 132 AYI82_RS05045 116 AYI77_RS09385 116
BN1227_RS21255 116 AYI97_RS14305 116 AYI82_RS05825 132 AYI77_RS20835 132
FlgC BN1227_RS06905 138 AYI97_RS06575 138 AYI82_RS05040 136 AYI77_RS09390 136
BN1227_RS21250 136 AYI97_RS14300 136 AYI82_RS05820 138 AYI77_RS20830 138
FlgD BN1227_RS21245 221 AYI97_RS06570 227 AYI82_RS05035 221 AYI77_RS09395 221
    AYI97_RS14295 221 AYI82_RS05815 227 AYI77_RS20825 227
FlgE BN1227_RS06915 453 AYI97_RS06565 453 AYI82_RS05810 453 AYI77_RS20820 453
FlgF BN1227_RS06920 247 AYI97_RS06560 247 AYI82_RS05805 247 AYI77_RS20815 247
FlgG BN1227_RS06925 262 AYI97_RS06555 262 AYI82_RS05020 261 AYI77_RS09410 261
BN1227_RS21230 261 AYI97_RS14280 261 AYI82_RS05800 262 AYI77_RS20810 262
FlgH BN1227_RS06930 224 AYI97_RS06550 363 AYI82_RS05015 223 AYI77_RS09415 223
BN1227_RS21225 223 AYI97_RS14275 224
223		 AYI82_RS05795 224 AYI77_RS20805 224
FlgI BN1227_RS06935 363 AYI97_RS06545 363 AYI82_RS05010 373 AYI77_RS09420 359
BN1227_RS21220 373 AYI97_RS14270 373 AYI82_RS05790 363 AYI77_RS20800 363
FlgJ BN1227_RS06940 336 AYI97_RS06540 336 AYI82_RS05785 336 AYI77_RS20795 336
FlgK BN1227_RS06945 641 AYI97_RS06535 641 AYI82_RS05000 456 AYI77_RS09430 456
BN1227_RS21210 456 AYI97_RS14260 456 AYI82_RS05780 641 AYI77_RS20790 641
FlgL BN1227_RS06950 401 AYI97_RS06530 401 AYI82_RS05775 401 AYI77_RS20785  
FlgM BN1227_RS06880 106 AYI97_RS06600 106 AYI82_RS05055 94 AYI77_RS09375 94
BN1227_RS21265 94 AYI97_RS14315 94 AYI82_RS05845 106 AYI77_RS20855 106
FlgN BN1227_RS06875 143 AYI97_RS06605 143 AYI82_RS05060 171 AYI77_RS09370 171
AYI82_RS05850 143 AYI77_RS20860 143
FlgP BN1227_RS06870 155 AYI97_RS06610 155 AYI82_RS05855 155 AYI77_RS20865 155
FlgT BN1227_RS06860 385 AYI97_RS06620 385 AYI82_RS05865 385 AYI77_RS20875 385
FliA BN1227_RS07090 239 AYI97_RS06390 239 AYI82_RS04955 236 AYI77_RS20445 239
BN1227_RS21165 236 AYI97_RS14215 236 AYI82_RS05635 239 AYI77_RS09475 236
FliD BN1227_RS06970 456 AYI97_RS06510 456 AYI82_RS04980 445 AYI77_RS20325 451
BN1227_RS21190 445 AYI97_RS14240 445 AYI82_RS05755 456    
FliE BN1227_RS07000 110 AYI97_RS06480 110 AYI82_RS05090 111 AYI77_RS09340 111
BN1227_RS21300 111 AYI97_RS14350 111 AYI82_RS05725 110 AYI77_RS20355 110
FliF BN1227_RS07005 569 AYI97_RS06475 569 AYI82_RS05085 555 AYI77_RS09345 555
BN1227_RS21295 555 AYI97_RS14345 555 AYI82_RS05720 569 AYI77_RS20360 569
FliG BN1227_RS07010 347 AYI97_RS06470 347 AYI82_RS05080 328 AYI77_RS09350 324
BN1227_RS21290 328 AYI97_RS14340 328 AYI82_RS05715 347 AYI77_RS20365 347
FliH BN1227_RS07015 322 AYI97_RS06465 324 AYI82_RS05710 324 AYI77_RS20370 324
FliI BN1227_RS07020 446 AYI97_RS06460 446 AYI82_RS05070 441 AYI77_RS09360 441
BN1227_RS21280 441 AYI97_RS14330 441 AYI82_RS05705 446 AYI77_RS20375 446
FliJ BN1227_RS07025 149 AYI97_RS06455 149 AYI82_RS05700 149 AYI77_RS20380 149
FliL BN1227_RS00740 135 AYI97_RS06445 174 AYI82_RS04960 145 AYI77_RS11650 135
BN1227_RS07035 174 AYI97_RS14220 145 AYI82_RS05690 174 AYI77_RS20390 174
BN1227_RS21170 145 AYI97_RS17155 135 AYI82_RS09710 135    
FliM BN1227_RS07040 342 AYI97_RS06440 342 AYI82_RS05685 342 AYI77_RS18030 238
BN1227_RS21315 300 AYI97_RS14365 300 AYI77_RS20395 342
FliN BN1227_RS07045 126 AYI97_RS06435 126 AYI82_RS05110 114 AYI77_RS18025 114
BN1227_RS21320 114 AYI97_RS14370 114 AYI82_RS05680 126 AYI77_RS20400 126
FliO BN1227_RS07050 119 AYI97_RS06430 119 AYI82_RS05675 119 AYI77_RS20405 119
FliP BN1227_RS07055 247 AYI97_RS06425 247 AYI82_RS05115 265 AYI77_RS18020 265
BN1227_RS21325 265 AYI97_RS14375 265 AYI82_RS05670 247 AYI77_RS20410 247
FliQ BN1227_RS07060 89 AYI97_RS06420 89 AYI82_RS05120 89 AYI77_RS18015 89
BN1227_RS21330 89 AYI97_RS14380 89 AYI82_RS05665 89 AYI77_RS20415 89
FliR BN1227_RS07065 265 AYI97_RS06415 265 AYI82_RS05125 259 AYI77_RS18010 259
BN1227_RS21335 259 AYI97_RS14385 259 AYI82_RS05660 265 AYI77_RS20420 265
FliS BN1227_RS06980 136 AYI97_RS06500 136 AYI82_RS04975 126 AYI77_RS09455 126
BN1227_RS21185 126 AYI97_RS14235 126 AYI82_RS05745 136 AYI77_RS20335 136
flhA BN1227_RS21345 692 AYI97_RS14395 692 AYI82_RS05135 692 AYI77_RS18000 692
BN1227_RS07075 701 AYI97_RS06405 701 AYI82_RS05650 701 AYI77_RS20430 701
flhB BN1227_RS07140 105 AYI97_RS06340 105 AYI82_RS05585 105 AYI77_RS20960 105
BN1227_RS21340 376 AYI97_RS14390 376 AYI82_RS05130 376 AYI77_RS18005 376
BN1227_RS07070 378 AYI97_RS06410 378 AYI82_RS05655 378 AYI77_RS20425 378
flhF BN1227_RS07080 458 AYI97_RS06400 458 AYI82_RS05645 458 AYI77_RS20435 458
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4. Discussion

S. algae has become an emerging marine zoonotic pathogen world-wide [5]. The spectrum of S. algae infection is broad with considerable morbidity and mortality in compromised hosts [31, 32]. Thus, understanding genomic characterization of S. algae is important for determining molecular epidemiology, understanding its pathogenesis, identifying specific biomarkers, tracing evolution of these strains, and developing control strategy of these pathogens in host reservoirs. In this study, we investigated the core genetic structure underlying S. algae virulence. The pathogenicity and distribution patterns of the S. algae strains extended our understanding of their pathogenic potential.

Previous attempts have been made to report the basic features of the genome of S. algae from various sources [33, 34]. In the present study, we used comparative genomics to analyze chromosomal sequence of four isolates to determine the common genetic content and organization, unique virulence attributes, and evolutionary relationship with other strains. Whole-genome sequence analysis of S. algae detected the presence of chemotaxis gene cluster cheYZA operon that is conserved in the chemotactic bacteria [35]. Chemotaxis is a directed motility in response to concentration gradients of signals. The cheA was demonstrated to be essential for chemotaxis using a two-component pathway [36]. In brief, CheA phosphorylates cheY and then is dephosphorylated by the phosphatase cheZ [37]. Previous studies revealed that CheW and CheA share structural homology and bind to the same site on chemoreceptors [37]. CheW is essential to the activation of CheA and the formation of CheA-CheW complex [38]. Owing to the wide range of S. algae habitats, the drivers of its chemotaxis could be very diverse. Previous studies have demonstrated that pathogenic bacteria use chemotaxis to localize reservoirs. Further study would be needed to identify the microenvironments suit for S. algae and the trigger of its chemotaxis.

Biliary tract infection is main manifestation of S. algae infection, and bile resistance has been noted in pathogenic strains [31]. In the study we also identified genes associated with bile adaption. The exbBD gene encodes Ton energy transduction system implicated in the response to bile [39, 40]. We also detected galU, htpB, and wecA involved in bile resistance [41–43]. The results support an earlier genomic study suggesting a common mechanism of bile resistance in Shewanella.

Motility is one characteristic of S. algae [3]. We identified series of flagellar gene operons in S. algae genomes. These flagellar systems are unique and require more study regarding the evolution and organization. Hemolysis is a main pathogenic feature in S. algae [44]. The gene hlyA encodes RTX pore-forming toxin α-hemolysin, which alters membrane permeability and causes cell lysis in a variety of human and animal hosts [45].

5. Conclusions

In conclusion, this is one of the few studies tracking genetic background of putative virulence-related genes in S. algae. Although the number of strains was limited, we highlight the unique characteristics of core virulence determinants in these strains, as a high level of genomic conservation.

Acknowledgments

The authors acknowledge the Taiwan's Ministry of Science and Technology (106-2221-E-194-056-MY3 and 107-2221-E-194-030-MY2), Taichung Tzu Chi Hospital (TTCRD 109-15) and Taichung Veterans General Hospital (TCVGH-1093901C) for providing funding for this study.

Contributor Information

Yao-Ting Huang, Email: ythuang@cs.ccu.edu.tw.

Po-Yu Liu, Email: liupoyu@gmail.com.

Data Availability

The sequence data are publicly available in NCBI SRA database (accession number: ACCC [LVCY00000000.1], CHL [LVDF00000000.1], and YHL [LVDU00000000.1]).

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The sequence data are publicly available in NCBI SRA database (accession number: ACCC [LVCY00000000.1], CHL [LVDF00000000.1], and YHL [LVDU00000000.1]).

Articles from The Canadian Journal of Infectious Diseases & Medical Microbiology = Journal Canadien des Maladies Infectieuses et de la Microbiologie Médicale are provided here courtesy of Wiley

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