Mycobacterial Pan-Genome Analysis Suggests Important Role of Plasmids in the Radiation of Type VII Secretion Systems
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In mycobacteria, various type VII secretion systems corresponding to different ESX (ESAT-6 secretory) types, are contributing to pathogenicity, iron acquisition, and/or conjugation. In addition to the known chromosomal ESX loci, the existence of plasmid-encoded ESX systems was recently reported. To investigate the potential role of ESX-encoding plasmids on mycobacterial evolution, we analyzed a large representative collection of mycobacterial genomes, including both chromosomal and plasmid-borne sequences. Data obtained for chromosomal ESX loci confirmed the previous five classical ESX types and identified a novel mycobacterial ESX-4-like type, termed ESX-4-bis. Moreover, analysis of the plasmid-encoded ESX loci showed extensive diversification, with at least seven new ESX profiles, identified. Three of them (ESX-P clusters 1-3) were found in multiple plasmids, while four corresponded to singletons. Our phylogenetic and gene-order-analyses revealed two main groups of ESX types: 1) ancestral types, including ESX-4 and ESX-4-like systems from mycobacterial and non-mycobacterial actinobacteria and 2) mycobacteria-specific ESX systems, including ESX-1-2-3-5 systems and the plasmid-encoded ESX types. Synteny analysis revealed that ESX-P systems are part of phylogenetic groups that derived from a common ancestor, which diversified and resulted in the different ESX types through extensive gene rearrangements. A converging body of evidence, derived from composition bias-, phylogenetic-, and synteny analyses points to a scenario in which ESX-encoding plasmids have been a major driving force for acquisition and diversification of type VII systems in mycobacteria, which likely played (and possibly still play) important roles in the adaptation to new environments and hosts during evolution of mycobacterial pathogenesis.
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ESX/T7S systems are encoded in different sections of the mycobacterial chromosome and seem to have evolved by gene duplication and diversification from simpler systems shuffled around in actinobacterial and mycobacterial species, often mediated by plasmids encoding ESX/T7S elements and type IV secretion elements.
“These systems, encoded in different sections of the mycobacterial chromosome, seem to have evolved by gene duplication and diversification from simpler systems that were shuffled around in different actinobacterial and mycobacterial species, often mediated by plasmids encoding ESX/T7S elements as well as elements of type IV secretion systems (21)(22)(23).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [21]
Five ESX systems are encoded in the genome of M. tuberculosis, and this is the highest number found in mycobacteria so far; other mycobacterial species show fewer systems (e.g., M. marinum four, M. abscessus three).
“Five ESX systems are encoded in the genome of M. tuberculosis (16,18), and this number is the highest found in mycobacteria so far; other mycobacterial species show fewer systems (e.g., Mycobacterium marinum shows four systems and Mycobacterium abscessus shows three systems) (21,22).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [21]
ESX-4, ESX-3, and ESX-1 are present in most fast-growing and slow-growing mycobacteria, while ESX-2 and ESX-5 are found only in selected slow-growing mycobacteria and represent the most recently evolved systems.
“While ESX-4, ESX-3, and ESX-1 are present in most fast-growing and slowgrowing mycobacteria, ESX-2 and ESX-5 systems are found only in selected slow-growing mycobacteria and thus represent the most recently evolved systems (21,22).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [21]
The ESX-4 locus of M. abscessus is different from that of other species, as it does contain EccE4.
“However, the ESX-4 locus of M. abscessus is different from that of other species, as it does contain EccE4 (21).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [21]
ESX-4 is one of the least well-characterized ESX systems, although it is considered the most ancestral esx locus in mycobacteria.
“ESX-4 is one of the least well-characterized ESX systems, although it is considered the most ancestral esx locus in mycobacteria (21,82).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [21]
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Self-citationvan Winden, V. J. C., Damen, M. P. M., Ummels, R., Bitter, W., & Houben, E. N. G. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.007090 · Cited by 15 · see citing works
- Authors
- Dumas, E., Christina Boritsch, E., Vandenbogaert, M., Rodríguez de la Vega, R. C., Thiberge, J.-M., Caro, V., Gaillard, J.-L., Heym, B., Girard-Misguich, F., Brosch, R., & Sapriel, G.
- Affiliations
- Inserm (FR)
- Institut Pasteur (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Brosch, Roland
- Sapriel, Guillaume
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-01-08
- Volume
- 8
- Issue
- 2
- Pages
- 387-402
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC4779608
- OpenAlex
- W2223993952
- Cited by
- 112
- References
- 70
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 8 · 2023: 4 · 2022: 14 · 2021: 26 · 2020: 10 · 2019: 10 · 2018: 8 · 2017: 10 · 2016: 7
- FWCI
- 10.76
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-14-JAMR-001-02, ANR-14-JAMR-0001)
- Institut National de la Santé et de la Recherche Médicale
- Horizon 2020 Framework Programme (H2020-PHC-643381, 260872, 643381)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- mycobacteria, type VII secretion system, pan-genome, gene order, synteny, gene rearrangement, actinobacteria, pathogenesis, iron acquisition, conjugation
- MeSH terms
- Type IV Secretion Systems, Mycobacterium, Phylogeny, Plasmids, Gene Rearrangement, Genome, Bacterial, Evolution, Molecular, Gene Transfer, Horizontal, Synteny
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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