Insights from the genome sequence of mycobacterium paragordonae, a potential novel live vaccine for preventing mycobacterial infections: The putative role of type VII secretion systems for an intracellular lifestyle within free-living environmental predators

Byoung Jun Kim, Ga Yeong Cha, Bo Ram Kim, Yoon Hoh Kook, Bum Joon Kim

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Mycobacterium paragordonae (Mpg) is a temperature-sensitive Mycobacterium species that can grow at permissive temperatures but fails to grow above 37C. Due to this unique growth trait, Mpg has recently been proposed as a novel live vaccine candidate for the prevention of mycobacterial infections. Furthermore, the increasing frequency of the isolation of Mpg from water supply systems led us to hypothesize that the free-living amoeba system is the natural reservoir of Mpg. In this study, we report the complete 6.7-Mb genome sequence of Mpg and show that this genome comprises four different plasmids with lengths of 305 kb (pMpg-1), 144 kb (pMpg-2), 26 kb (pMpg-3), and 17 kb (pMpg-4). The first two plasmids, pMpg-1 and -2, encode distinct Type VII secretion systems (T7SS), ESX-P5 and ESX-2, respectively. Genome-based phylogeny indicated that Mpg is the closest relative to M. gordonae, which has a 7.7-Mb genome; phylogenetic analysis revealed an average of 86.68% nucleotide identity between these two species. The most important feature of Mpg genome is the acquisition of massive genes related to T7SS, which may have had effect on adaptation to their intracellular lifestyle within free-living environmental predators, such as amoeba. Comparisons of the resistance to bacterial killing within amoeba indicated that Mpg exhibited stronger resistance to amoeba killing compared to M. gordonae and M. marinum, further supporting our genome-based findings indicating the special adaptation of Mpg to free-living amoeba. We also determined that, among the strains studied, there were more shared CDS between M. tuberculosis and Mpg. In addition, the presence of diverse T7SSs in the Mpg genome, including an intact ESX-1, may suggest the feasibility of Mpg as a novel tuberculosis vaccine. Our data highlight a significant role of lateral gene transfer in the evolution of mycobacteria for niche diversification and for increasing the intracellular survival capacity.

Original languageEnglish
Article number1524
JournalFrontiers in Microbiology
Volume10
Issue numberJUL
DOIs
StatePublished - 1 Jan 2019

Fingerprint

Mycobacterium
Life Style
Vaccines
Genome
Infection
Amoeba
Gordonia Bacterium
Type VII Secretion Systems
Plasmids
Tuberculosis Vaccines
Horizontal Gene Transfer
Temperature
Water Supply
Phylogeny
Mycobacterium tuberculosis
Nucleotides

Keywords

  • Genome sequence
  • Lateral gene transfer
  • M. gordonae
  • Mycobacterium paragordonae
  • Type VII secretion systems

Cite this

@article{8761934b2b584aec84e625d309e14435,
title = "Insights from the genome sequence of mycobacterium paragordonae, a potential novel live vaccine for preventing mycobacterial infections: The putative role of type VII secretion systems for an intracellular lifestyle within free-living environmental predators",
abstract = "Mycobacterium paragordonae (Mpg) is a temperature-sensitive Mycobacterium species that can grow at permissive temperatures but fails to grow above 37◦C. Due to this unique growth trait, Mpg has recently been proposed as a novel live vaccine candidate for the prevention of mycobacterial infections. Furthermore, the increasing frequency of the isolation of Mpg from water supply systems led us to hypothesize that the free-living amoeba system is the natural reservoir of Mpg. In this study, we report the complete 6.7-Mb genome sequence of Mpg and show that this genome comprises four different plasmids with lengths of 305 kb (pMpg-1), 144 kb (pMpg-2), 26 kb (pMpg-3), and 17 kb (pMpg-4). The first two plasmids, pMpg-1 and -2, encode distinct Type VII secretion systems (T7SS), ESX-P5 and ESX-2, respectively. Genome-based phylogeny indicated that Mpg is the closest relative to M. gordonae, which has a 7.7-Mb genome; phylogenetic analysis revealed an average of 86.68{\%} nucleotide identity between these two species. The most important feature of Mpg genome is the acquisition of massive genes related to T7SS, which may have had effect on adaptation to their intracellular lifestyle within free-living environmental predators, such as amoeba. Comparisons of the resistance to bacterial killing within amoeba indicated that Mpg exhibited stronger resistance to amoeba killing compared to M. gordonae and M. marinum, further supporting our genome-based findings indicating the special adaptation of Mpg to free-living amoeba. We also determined that, among the strains studied, there were more shared CDS between M. tuberculosis and Mpg. In addition, the presence of diverse T7SSs in the Mpg genome, including an intact ESX-1, may suggest the feasibility of Mpg as a novel tuberculosis vaccine. Our data highlight a significant role of lateral gene transfer in the evolution of mycobacteria for niche diversification and for increasing the intracellular survival capacity.",
keywords = "Genome sequence, Lateral gene transfer, M. gordonae, Mycobacterium paragordonae, Type VII secretion systems",
author = "Kim, {Byoung Jun} and Cha, {Ga Yeong} and Kim, {Bo Ram} and Kook, {Yoon Hoh} and Kim, {Bum Joon}",
year = "2019",
month = "1",
day = "1",
doi = "10.3389/fmicb.2019.01524",
language = "English",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A.",
number = "JUL",

}

TY - JOUR

T1 - Insights from the genome sequence of mycobacterium paragordonae, a potential novel live vaccine for preventing mycobacterial infections

T2 - The putative role of type VII secretion systems for an intracellular lifestyle within free-living environmental predators

AU - Kim, Byoung Jun

AU - Cha, Ga Yeong

AU - Kim, Bo Ram

AU - Kook, Yoon Hoh

AU - Kim, Bum Joon

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Mycobacterium paragordonae (Mpg) is a temperature-sensitive Mycobacterium species that can grow at permissive temperatures but fails to grow above 37◦C. Due to this unique growth trait, Mpg has recently been proposed as a novel live vaccine candidate for the prevention of mycobacterial infections. Furthermore, the increasing frequency of the isolation of Mpg from water supply systems led us to hypothesize that the free-living amoeba system is the natural reservoir of Mpg. In this study, we report the complete 6.7-Mb genome sequence of Mpg and show that this genome comprises four different plasmids with lengths of 305 kb (pMpg-1), 144 kb (pMpg-2), 26 kb (pMpg-3), and 17 kb (pMpg-4). The first two plasmids, pMpg-1 and -2, encode distinct Type VII secretion systems (T7SS), ESX-P5 and ESX-2, respectively. Genome-based phylogeny indicated that Mpg is the closest relative to M. gordonae, which has a 7.7-Mb genome; phylogenetic analysis revealed an average of 86.68% nucleotide identity between these two species. The most important feature of Mpg genome is the acquisition of massive genes related to T7SS, which may have had effect on adaptation to their intracellular lifestyle within free-living environmental predators, such as amoeba. Comparisons of the resistance to bacterial killing within amoeba indicated that Mpg exhibited stronger resistance to amoeba killing compared to M. gordonae and M. marinum, further supporting our genome-based findings indicating the special adaptation of Mpg to free-living amoeba. We also determined that, among the strains studied, there were more shared CDS between M. tuberculosis and Mpg. In addition, the presence of diverse T7SSs in the Mpg genome, including an intact ESX-1, may suggest the feasibility of Mpg as a novel tuberculosis vaccine. Our data highlight a significant role of lateral gene transfer in the evolution of mycobacteria for niche diversification and for increasing the intracellular survival capacity.

AB - Mycobacterium paragordonae (Mpg) is a temperature-sensitive Mycobacterium species that can grow at permissive temperatures but fails to grow above 37◦C. Due to this unique growth trait, Mpg has recently been proposed as a novel live vaccine candidate for the prevention of mycobacterial infections. Furthermore, the increasing frequency of the isolation of Mpg from water supply systems led us to hypothesize that the free-living amoeba system is the natural reservoir of Mpg. In this study, we report the complete 6.7-Mb genome sequence of Mpg and show that this genome comprises four different plasmids with lengths of 305 kb (pMpg-1), 144 kb (pMpg-2), 26 kb (pMpg-3), and 17 kb (pMpg-4). The first two plasmids, pMpg-1 and -2, encode distinct Type VII secretion systems (T7SS), ESX-P5 and ESX-2, respectively. Genome-based phylogeny indicated that Mpg is the closest relative to M. gordonae, which has a 7.7-Mb genome; phylogenetic analysis revealed an average of 86.68% nucleotide identity between these two species. The most important feature of Mpg genome is the acquisition of massive genes related to T7SS, which may have had effect on adaptation to their intracellular lifestyle within free-living environmental predators, such as amoeba. Comparisons of the resistance to bacterial killing within amoeba indicated that Mpg exhibited stronger resistance to amoeba killing compared to M. gordonae and M. marinum, further supporting our genome-based findings indicating the special adaptation of Mpg to free-living amoeba. We also determined that, among the strains studied, there were more shared CDS between M. tuberculosis and Mpg. In addition, the presence of diverse T7SSs in the Mpg genome, including an intact ESX-1, may suggest the feasibility of Mpg as a novel tuberculosis vaccine. Our data highlight a significant role of lateral gene transfer in the evolution of mycobacteria for niche diversification and for increasing the intracellular survival capacity.

KW - Genome sequence

KW - Lateral gene transfer

KW - M. gordonae

KW - Mycobacterium paragordonae

KW - Type VII secretion systems

UR - http://www.scopus.com/inward/record.url?scp=85069001128&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2019.01524

DO - 10.3389/fmicb.2019.01524

M3 - Article

AN - SCOPUS:85069001128

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - JUL

M1 - 1524

ER -