ESAT6 secretion (ESX; also known as type VII secre-
tion) systems are bacterial secretion systems that are
named after the first identified effector, the 6 kDa
early secretory antigenic target (ESAT6; also known as
EsxA), of Mycobacterium tuberculosis, the aetiological
agent of human tuberculosis
1,2
. ESX systems are found
in mycobacteria and various other genera in the phylum
Actinobacteria
3,4
, such as Streptomyces, Corynebacterium,
Nocardia or Gordonia, and more distantly related ESX-
like systems also exist in Gram-positive bacteria in the
phylum Firmicutes, including in Bacillus anthracis
5
,
Bacillus subtilis
6,7
, Staphylococcus aureus
8,9
and Listeria
monocytogenes
10
(BOX 1). In mycobacteria, ESX systems
function as specialized secretion systems that enable the
transport of selected substrates across the complex, thick
mycobacterial cell envelope that forms a structural bar-
rier to protein export
11
. The thickness and complexity
of the envelope, which provides protection to myco-
bacteria under harsh environmental conditions, are due
to the presence of mycolic acids that are linked, usually
covalently, to an arabinogalactan–peptidoglycan matrix, as
well as various extractable lipids, polysaccharides, lipo-
glycans and proteins that are not covalently attached to
the matrix and that may vary among species
12
.
Two characteristics unify all esx loci across the differ-
ent phyla. First, the presence of genes that encode small
secreted proteins of approximately 100 amino acids
that have a conserved Trp-X-Gly (WXG) motif, which
contributes to the formation of helix–turn–helix struc-
tures
13
, in the centre of the polypeptide; and, second, the
presence of genes that encode transmembrane proteins
of the FtsK–SpoIIIE-like ATPase family
14
. The most well-
known proteins that contain the WXG motif are EsxA
of M. tuberculosis and its adjacently encoded hetero-
dimerization partner EsxB (also known as CFP10)
15
.
Apart from these core characteristics, ESX systems are
quite diverse, which suggests that they have been shaped
by a long evolutionary process that has involved gene
duplication and diversification
3,16,17
, as well as horizontal
gene transfer between chromosomes and plasmids of
different bacterial species and genera
4,18
(BOX 2).
Of the five ESX systems that have been described in
M. tuberculosis (ESX-1, ESX-2, ESX-3, ESX-4 and ESX-5;
FIG. 1a), at least three are required for full virulence. The
first ESX system (ESX-1) was identified in parallel by
different comparative and functional genomic studies
that involved M. tuberculosis and the attenuated vaccine
strains Mycobacterium bovis bacille Calmette–Guérin
(BCG) and Mycobacterium microti
19–24
. The vaccine
strains lack EsxA, owing to spontaneous deletions of dif-
ferent sized portions of the esx‑1 locus, each of which is
known as region of difference 1 (RD1) for the respective
strain
25,26
(FIG. 1a). ESX-1 in M. tuberculosis has subse-
quently been shown to be essential for resistance to, and
evasion of, host responses. One of the key functions of
ESX-1 is its role in the induction of phagosomal rupture,
which releases bacteria and/or bacterial products into
the cytosolic compartment of host phagocytes. The sens-
ing of bacterial products, such as DNA, triggers a com-
plex signalling cascade of the innate immune system,
Actinobacteria
A phylum of Gram-positive
bacteria that is characterized
by high GC content.
Mycolic acids
Long-chain (C
60
–C
90
) fatty acids
that are specifically found in
the mycobacterial cell
envelope; together with
extractable lipids, mycolic
acids form the mycobacterial
outer membrane (also known
as the mycomembrane).
ESX secretion systems: mycobacterial
evolution to counter host immunity
Matthias I. Gröschel
1,2
, Fadel Sayes
1
, Roxane Simeone
1
, Laleh Majlessi
1
and Roland Brosch
1
Abstract | Mycobacterium tuberculosis uses sophisticated secretion systems, named 6 kDa early
secretory antigenic target (ESAT6) protein family secretion (ESX) systems (also known as type VII
secretion systems), to export a set of effector proteins that helps the pathogen to resist or evade
the host immune response. Since the discovery of the esx loci during the M. tuberculosis H37Rv
genome project, structural biology, cell biology and evolutionary analyses have advanced our
knowledge of the function of these systems. In this Review, we highlight the intriguing roles that
these studies have revealed for ESX systems in bacterial survival and pathogenicity during
infection with M. tuberculosis. Furthermore, we discuss the diversity of ESX systems that has been
described among mycobacteria and selected non-mycobacterial species. Finally, we consider
how our knowledge of ESX systems might be applied to the development of novel strategies for
the treatment and prevention of disease.
1
Institut Pasteur, Unit for
Integrated Mycobacterial
Pathogenomics, Paris 75724,
Cedex 15, France.
2
Department of Pulmonary
Diseases & Tuberculosis,
University Medical Center
Groningen, University
of Groningen, 9700 RB
Groningen, The Netherlands.
Correspondence to R.B.
roland.brosch@pasteur.fr
doi:10.1038/nrmicro.2016.131
Published online 26 Sep 2016
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