Genomic analysis of Latin American-Mediterranean family of <i>Mycobacterium tuberculosis</i> clinical strains from Kazakhstan

The human-adapted strains of the Mycobacterium tuberculosis complex (MTBC) comprise seven phylogenetic lineages originally associated with their geographical distribution. Here, we report the genomes of three drug-resistant clinical isolates of the Latin American-Mediterranean (LAM) family collected in Kazakhstan. We utilised whole-genome sequencing to study the distribution and drug resistance of these isolates. Phylogenetic analysis grouped the genomes described in this study with the sequences from Russia, Uzbekistan, and Kazakhstan belonging to the LAM family. One isolate has acquired extensive drug resistance to seven antituberculosis drugs. Our results suggest at least two multi-drug resistant (MDR)/extensively drug-resistant (XDR)-associated genotypes of the LAM family circulate in Kazakhstan.

Key words:
Mycobacterium tuberculosis; genome; tuberculosis; phylogeny

Authorship

Pavel Tarlykov ⁺+ Corresponding author: tarlykov@biocenter.kz

National Center for Biotechnology, Nur-Sultan, KazakhstanNational Center for BiotechnologyKazakhstanNur-Sultan, KazakhstanNational Center for Biotechnology, Nur-Sultan, Kazakhstan

http://orcid.org/0000-0003-2075-307X

Sabina Atavliyeva

National Center for Biotechnology, Nur-Sultan, KazakhstanNational Center for BiotechnologyKazakhstanNur-Sultan, KazakhstanNational Center for Biotechnology, Nur-Sultan, Kazakhstan

Arike Alenova

National Scientific Center for Phthisiopulmonology, Almaty, KazakhstanNational Scientific Center for PhthisiopulmonologyKazakhstanAlmaty, KazakhstanNational Scientific Center for Phthisiopulmonology, Almaty, Kazakhstan

Yerlan Ramankulov

National Center for Biotechnology, Nur-Sultan, KazakhstanNational Center for BiotechnologyKazakhstanNur-Sultan, KazakhstanNational Center for Biotechnology, Nur-Sultan, Kazakhstan

+ Corresponding author: tarlykov@biocenter.kz

PT and YR conceived the study; PT and AA designed the study protocol; AA assisted in the culture work; SA and PT performed the sequencing; PT and SA analysed the data; PT and SA wrote the manuscript. The authors declare no conflict of interest, financial, or other.

SCIMAGO INSTITUTIONS RANKINGS

National Center for Biotechnology, Nur-Sultan, KazakhstanNational Center for BiotechnologyKazakhstanNur-Sultan, KazakhstanNational Center for Biotechnology, Nur-Sultan, Kazakhstan

Figures | Tables

Figures (1)
Tables (3)

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Maximum-likelihood phylogeny of three Mycobacterium tuberculosis isolates from this study and 81 representative genomes of M. tuberculosis complex (MTBC) strains. Sublineages are labeled according to Coll et al.²2. Coll F, McNerney R, Guerra-Assunção JA, Glynn JR, Perdigao J, Viveiros M, et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat Commun. 2014; 5: 4812. Branch lengths are proportional to nucleotide substitutions and the topology is rooted with Mycobacterium canettii. Three isolates from this study are highlighted. Bootstrap values are shown.

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TABLE I
Characteristics of three Mycobacterium tuberculosis genome assemblies

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TABLE II
Mutations observed in drug resistance-associated loci of the Mycobacterium tuberculosis isolates

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TABLE III
Latin American-Mediterranean(LAM) sublineages and spoligotype international types (SITs) in Mycobacterium tuberculosis isolates from Kazakhstan based on the whole-genome sequences (WGS) data

Maximum-likelihood phylogeny of three Mycobacterium tuberculosis isolates from this study and 81 representative genomes of M. tuberculosis complex (MTBC) strains. Sublineages are labeled according to Coll et al.²2. Coll F, McNerney R, Guerra-Assunção JA, Glynn JR, Perdigao J, Viveiros M, et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat Commun. 2014; 5: 4812. Branch lengths are proportional to nucleotide substitutions and the topology is rooted with Mycobacterium canettii. Three isolates from this study are highlighted. Bootstrap values are shown.

TABLE I Characteristics of three Mycobacterium tuberculosis genome assemblies

Isolate	Platform	SRA accession No.	Genome size (bp)	GC content (%)	Coverage (x)	No. of contigs	Total no. of CDSs	SNPs called*
3538	MiSeq**	SRR11241401	4,427,028	65.24	130	404	4,392	1455
4142	MiSeq	SRR11241400	4,351,634	65.58	116	243	4,237	1185
4330	Ion Torrent***	SRR11241402	4,344,962	65.00	84	925	4,495	989

*: compared to the genome of reference strain H37Rv (GenBank accession no. NC_000962.3); **: MiSeq libraries were prepared using a Nextera DNA Flex Library Prep Kit and the sequencing was performed using MiSeq Reagent Kit v3; ***: Ion Torrent library was prepared using an Ion Xpress Plus fragment library kit and the sequencing was conducted using a 318 Chip. CDSs: coding sequences; GC: guanine-cytosine; SRA: sequence read archive.

TABLE II Mutations observed in drug resistance-associated loci of the Mycobacterium tuberculosis isolates

Isolate	Drug resistance
Isolate	AMI	EMB	INH	OFX	PZA	RIF	SM	ETH
3538
Gene			katG			rpoB
AA change			Ser315Thr			Ser450Leu
Base change			G/C 944			C/T 1349
% of reads			100			100
4142
Gene	rrs	embB	katG	gyrA		rpoB	rrs	fabG
AA change	-	Met306Ile	Ser315Thr	Asp94Tyr		His445Leu	-	-
Base change	A/G 1401	G/C 918	G/C 944	G/T 280		A/T 1334	A/C 514	C/T -15
% of reads	100	100	100	100		99	96	100
4330
Gene		embB	katG			rpoB	rrs	fabG
AA change		Met306Ile	Ser315Thr			His445Leu	-	-
Base change		G/C 918	G/C 944			A/T 1334	A/C 514	C/T -15
% of reads		98	99			100	99	100

AMI: amikacin; EMB: ethambutol; INH: isoniazid; OFX: ofloxacin; PZA: pyrazinamide; RIF: rifampin; SM: streptomycin; ETH: ethambutol.

TABLE III Latin American-Mediterranean(LAM) sublineages and spoligotype international types (SITs) in Mycobacterium tuberculosis isolates from Kazakhstan based on the whole-genome sequences (WGS) data

Isolate	Year	Sublineage*	RD	SIT	IS6110 (plcA gene) LAM-RUS	Resistance	Reference
3538	2014	L4.3.3	RD115	42	-	MDR	This study
4142	2014	L4.3.3	RD115	42	+	XDR	This study
4330	2014	L4.3.3	RD115	42	+	MDR	This study
G04485	2002	L4.3.3	RD115	42	-	MDR	Stucki et al.
G04546	2007	L4.3.3	RD115	254	+	S	Stucki et al.
G04493	2011	L4.3.3	RD115	444	+	S	Stucki et al.

*: sublineage classification based on Coll et al.⁽²⁾; MDR: multi-drug resistant isolate; XDR: extensively drug-resistant isolate; S: sensitive isolate.

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Genomic analysis of Latin American-Mediterranean family of <i>Mycobacterium tuberculosis</i> clinical strains from Kazakhstan

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[1] + Corresponding author: tarlykov@biocenter.kz