Diversity of Mycolactone-Producing Mycobacteria: History
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Contributor:
Marine Combe
,
Emira Cherif
,
Romain Blaizot
,
Damien Breugnot
,
Rodolphe Elie Gozlan

Buruli ulcer (BU), a human necrotizing skin disease mainly affecting tropical and subtropical areas, commonly admitted to be caused by Mycobacterium ulcerans worldwide although other mycolactone-producing mycobacteria and even mycobacterium species were found associated with BU or BU-like cases. 

  • molecular testing
  • Buruli ulcer (BU)
  • Mycobacterium ulcerans

1. Introduction

The Buruli ulcer (BU) is a human necrotizing skin disease that affects between 5000 and 6000 people annually across 33 countries worldwide, mainly located in tropical and subtropical areas [1]. BU represents the third most common mycobacterial disease after tuberculosis and leprosy [2] and is responsible for severe morbidity and mortality mainly in low-resources human populations living near contaminated water bodies [1]. Clinical signs of the disease include painless nodules, plaques and edema, followed by the development of skin ulcers that can lead to osteomyelitis and permanent disability if early detection and appropriate treatment are delayed or absent [3][4]. BU and its infectious etiological agent Mycobacterium ulcerans (previously described as M. buruli), also belonging to the mycolactone-producing mycobacteria (MPM) complex, were first described by MacCallum, Buckle, Tolhurst and Sissons in 1948 [5] from six cases of skin ulceration occurring in Australia on the basis of histology, pathogenicity, culture and microscopy of M. ulcerans. But the first molecular tests targeting M. ulcerans DNA were developed years later [2][6][7]. Since then, M. ulcerans is generally considered the only species responsible for BU worldwide and most studies have used three genetic markers to detect its DNA from human ulcerations, animal and environmental samples (IS2404, IS2606, KR-B). However, the genetic distinction between M. ulcerans and other MPM also sharing very similar clinical characteristics, namely M. shinshuense, M. pseudoshottsii, M. liflandii, M. marinum [8][9], based on these three commonly used molecular tests remains impossible. However, all MPM share the ability to cause a BU-like disease in humans and carefully identifying the etiological agent causing disease has major implications for BU diagnosis and the choice for the antibiotherapy. Importantly, it has been shown that M. ulcerans and other MPM are genetically related enough to form a single species complex, all representing variants rather than different species [9][10][11][12]. More recently, M. shinshuense, M. marinum and M. liflandii were found in BU-like cases diagnosed in Japan [13][14], Côte d’Ivoire (Africa) [15] and French Guiana (South America) [16], respectively. Interestingly, in Côte d’Ivoire Nguetta et al. [15] also found other mycobacteria, not belonging to the MPM complex, associated with BU-like cases, such as M. chelonae and M. smegmatis, and M. gilvum was found associated with some BU-like cases in French Guiana [17]. Taken together, these results suggest that (1) all MPM should definitely be considered variants of the same MPM complex and (2) all MPM variants or even other mycobacteria species apparently not producing mycolactone could cause either the same BU disease or slightly different skin ulcerations all diagnosed as BU to date.

2. History of BU Diagnosis and M. ulcerans DNA Testing

2.1. Clinical and Microbial Diagnosis

BU was initially diagnosed by clinical observations of ulceration and confirmed by microscopic findings of acid-fast bacilli (AFB) after Ziehl–Neelsen staining (resistance to acid and/or ethanol decolorization, BAAR: bacillus acido-alcohol-resistant), a characteristic of bacteria belonging to the Genus Mycobacterium. The use of specific serological tests was not suitable due to cross-reactivity between mycobacterial antigens [18]. In addition, M. ulcerans can be difficult to culture, especially from environmental samples, due to the long generation time of the pathogen (>48 h) and proliferation of other mycobacteria [2][10][19]. Also, primary cultures usually become positive after several months of incubation and many clinical BU cases are reported as culture negative. Consequently, the implementation of rapid molecular identification tools has been a major step in the diagnosis of BU [2][7].

2.2. First Molecular Diagnosis

While the first molecular distinctions between M. ulcerans, other MPM variants and other mycobacteria species were performed by analyzing 16S rRNA, hsp65 and/or rpoB gene sequences, these genetic markers were limited to small sequence fragments and were therefore insufficient to establish a strong phylogenetic relationship between species [6][20][21]. Portaels et al. [2] and Ross et al. [7] were the first to develop PCR assays for the detection of M. ulcerans. Although potential candidate genetic targets had been published, there were some problems: (1) the genus-specific 65-kDa heat shock protein antigen had a high degree of homology between different mycobacterial species [22][23] and was therefore not a good target for specific amplifications [7]; (2) the 16S rRNA sequence showed only a single nucleotide divergence between the M. ulcerans variant and M. marinum [20], and it showed variability between different strains of the M. ulcerans [6] and was thus unsuitable for developing a simple, sensitive and specific PCR-based test.

2.3. Discovery and Implementation of IS2404 and IS2606 PCR Assays

Ross et al. [7] searched for a new and more specific DNA sequence in the M. ulcerans variant genome and therefore screened a genomic library of DNA fragments after digestion with AluI and HaeIII. Southern blot hybridization using a M. ulcerans genomic probe revealed a band of approximately 1.1 kb that was highly reactive in AluI-digested DNA, which appeared to be repeated at least 50 times in the M. ulcerans variant genome and therefore was considered as an ideal target for the PCR-based test [7]. This PCR test (primer pair MU1 and MU2, amplify between tandem copies of IS2404) was rapidly used for the diagnosis of BU human cases [7] as well as for the detection of the M. ulcerans variant in the environment [24]. These authors showed that the length of the complete repeat element was 1274 bp, flanked by 7-bp direct repeats with 12-bp terminal inverted repeats and a single large open reading frame potentially encoding a protein composed of 328 amino acids [25]. Their results suggested that this repeat element may constitute an insertion sequence (IS) element, which is commonly found in other mycobacteria and usually used as a template for PCR amplifications [25]. This repeat was named IS2404 (amplified with primer pairs MU5 and MU6). They also discovered another insertion element of 1404 bp in length with 12-bp terminal inverted repeats, repeated between 30–40 times per genome, with a single open reading frame potentially encoding a protein of 445 amino acids that they named IS2606 (amplified with primer pairs MU7 and MU8) [25]. IS2404 and IS2606 appeared to be unrelated to and distinct from other known mycobacterial IS, such as IS1245 found in M. avium [26] and IS1512 found in M. gordonae [27]. At that time, specificity tests of the IS2404 and IS2606 PCR assays showed that IS2404 was specific to the M. ulcerans variant, while IS2606 was also present in the genome of M. lentiflavum which is not phylogenetically related to M. ulcerans [25].

2.4. Implementation of qPCR Assays

The IS-based PCR tests, particularly IS2404, have become the molecular basis for the detection of the M. ulcerans variant from which more recent studies have attempted to improve their specificity and sensitivity [28], notably through the implementation of the quantitative real-time PCR (qPCR) combined with the use of TaqMan probes that allow (1) confirmation of the identity of a DNA amplification product and (2) simultaneous amplification of multiple DNA targets [29][30].

3. Implication for the Diagnosis and Treatment of BU

3.1. Implication for BU Diagnosis

BU has a wide spectrum of clinical manifestations [31], with extremely aggressive infections in some areas while others are indolent or rapidly healing [6]. These observations have raised the hypothesis that if, in a given area, M. ulcerans is genotypically homogeneous, then host factors such as immunity, metabolism and nutrition may play an important role in the history of infection [6]. However, while MPM variants were initially given different species names based on slightly different phenotypic characteristics, they all show great genotypic similarities making it clear that they represent rather variants of the same MPM complex. This means that a variety of MPM variants are capable of causing similar skin ulcerations all named BU, a scenario that could also explain the spectrum of clinical observations. This hypothesis is notably supported by the association of clinically diagnosed BU cases with M. liflandii or M. liflandii-like variants [16][32] or M. marinum variants [33]. In these cases, IS2404 and KR-B PCR were both positive. While some studies reported negative cultures for the M. liflandii variant [32] others described positive cultures with phenotypic features similar to the M. ulcerans variant such as slow growth (>6 weeks), yellowish coloration and granular appearance of the colonies [16]. Then, whilst M. liflandii and M. pseudoshottsii variant infections have been mainly reported in frogs and fish, respectively, these germs may be under-detected in human lesions and should be looked for in order to determine their pathogenicity. Nevertheless, it is also important to keep in mind that although M. marinum variant infections can be mistaken for BU, they usually present specific clinical syndromes such as verrucous plaques or sporotrichoid lesions which are not typical of M. ulcerans variant infections [34]. It is also noteworthy that even in lesions mimicking stricto sensu BU, M. marinum variant lesions do not present undermined edges, which are the most specific sign of M. ulcerans variant infections. Therefore, it is necessary to bear in mind that some strains of M. marinum can also be responsible for a different nosological entity (the so-called “fish-tank disease”). Also, whilst M. shinshuense and M. ulcerans variant infections are characterized by similar clinical presentations, an aquatic exposure does not seem to be relevant in M. shinshuense variant transmission [35].
Has BU been underestimated? Since clinical diagnosis is usually based on careful examination of the ulceration and then confirmed either by IS2404 PCR amplification and/or direct microscopy and/or histopathology (including AFB staining, a characteristic shared by all mycobacteria; [36]) and/or culture, it seems that the answer is no. However, the genetic diversity of the mycobacterium capable of causing BU or BU-like disease has been underestimated.

3.2. Implication for M. ulcerans Genetic Diversity

Another question remains: do these MPM variants represent the genetic diversity of M. ulcerans? Some authors have suggested that the M. ulcerans variant has recently passed through an evolutionary bottleneck and adapted to a new niche environment [10]. Tobias et al. [9] referred to “niche-adapted” mycobacteria, with M. liflandii and M. ulcerans variants representing thus different ecotypes. Interestingly, it found both variants in the same environmental habitats (sediments) in French Guiana as well as in BU biopsies [16], suggesting that these MPM variants share the same environments. Since BU is known to be caused by the M. ulcerans variant worldwide, scholars propose to consider that all other variants belonging to the MPM complex represent M. ulcerans’ variability. Nevertheless, scholars do not exclude that within this MPM complex the M. ulcerans variant did not appear first but rather evolved from another ancestor variant. Notably, based on the number of ISs repeats (IS2404 and IS2606) and the number of pseudogenes present in the MPM genomes, scholars suggest that they could have evolved from an ancestor variant to adapt to the host they infect rather than to an ecological niche.

3.3. What about the Pathogenicity of Other Mycobacterium Species

Another important finding is the discovery of other mycobacterial species (not belonging to the MPM complex) associated with diagnosed BU cases. Stinear et al. [19] showed that out of 50 clinical samples diagnosed as BU, only 40 were positives for IS2404, raising the question about the etiology of the others. In Côte d’Ivoire, M. chelonae and M. smegmatis have been found in BU lesions [15] and more recently based on metabarcoding analysis of clinical samples, M. gilvum has been found associated with some BU cases in French Guiana [17]. For the latter cases, AFB (BAAR) staining was negative, IS2404 and KR-B qPCR were both negative, and the culture on LJ solid medium was negative [17]. As it has shown that M. gilvum does not harbor IS2404, IS2606 and KR-B in its genome and plasmids (Figure 1), this raises questions about its mechanisms of pathogenicity in humans. Taken together, these results raise the possibility that other mycobacterial species may have other types of virulence genes and immunosuppressive properties as the MPM variants that enable them to cause skin ulcerations similar to those caused by MPM variants. Furthermore, these results highlight the potential of metabarcoding studies, usually used for environmental investigations, in the search for the infectious agent responsible for human disease. These broader molecular screens could, for example, help the medical community target the most appropriate treatment and thus avoid late responses to inappropriate antibiotic therapy.

3.4. Implication for BU Treatment

The World Health Organization (WHO) recommends a combination of rifampicin (10 mg/kg once daily) and clarithromycin (7.5 mg/kg twice daily) to treat BU [37]. In Australia, although not proven effective, a combination of rifampicin (10 mg/kg once daily) and moxifloxacin or ciprofloxacin (400 mg once daily) is routinely used to treat patients (WHO, 2022). In Japan, a triple combination of rifampicin, levofloxacin and clarithromycin is used [38] while in French Guiana, treatment consists of a combination of rifampicin, amikacin or clarithromycin [39]. Whilst all based on rifampicin, BU treatment also combines other antimicrobial molecules that are variable upon the region. Rifampicin inhibits bacterial DNA synthesis through the inhibition of the DNA-dependent RNA polymerase [40]. However, some M. ulcerans variants previously showed resistance to rifampicin after monotherapy, suggesting that this mycobacterium has the ability to develop resistance against antimicrobial drugs commonly used to treat BU [41]. Whilst rifampicin and rifabutin have been shown to be the most active drugs against M. marinum variant infections [42] they are often treated with tritherapies including rifampicin, clarithromycin and ethambutol [43][44] thus slightly differing from M. ulcerans variant therapy. Amikacin, ciprofloxacin, kanamycin and lincomycin inhibited the growth of M. pseudoshottsii variant isolates [45]. In addition to being resistant to isoniazid, ethambutol and ethionamide, the M. liflandii variant also exhibits resistance to rifampicin (rifampin) and clarithromycin [46][47], suggesting that the combination of these later two antibiotics may not be appropriate to treat BU cases caused by M. liflandii variants. In French Guiana, M. gilvum infections were cured either after erysipelas treatment (based on penicillin administration) or with a combination of rifampicin (600 mg daily) and clarithromycin (500 mg twice daily) [17] while this mycobacterium has been shown to be resistant to isoniazid, sodium aminosalicylate and rifampicin [48]. These findings suggest that common combinations of antibiotic molecules locally used to treat BU might be inappropriately used depending on the variant/species causing disease.

This entry is adapted from the peer-reviewed paper 10.3390/ijms241813727

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