Genome analysis reveals three genomospecies in Mycobacterium abscessus
© Sassi and Drancourt; licensee BioMed Central Ltd. 2014
Received: 5 September 2013
Accepted: 30 April 2014
Published: 12 May 2014
Mycobacterium abscessus complex, the third most frequent mycobacterial complex responsible for community- and health care-associated infections in developed countries, comprises of M. abscessus subsp. abscessus and M. abscessus subsp. bolletii reviously referred as Mycobacterium bolletii and Mycobacterium massiliense. The diversity of this group of opportunistic pathogens is poorly described.
In-depth analysis of 14 published M. abscessus complex genomes found a pan-genome of 6,153 proteins and core-genome of 3,947 (64.1%) proteins, indicating a non-conservative genome. Analysing the average percentage of amino-acid sequence identity (from 94.19% to 98.58%) discriminates three main clusters C1, C2 and C3: C1 comprises strains belonging to M. abscessus, C2 comprises strains belonging to M. massiliense and C3 comprises strains belonging to M. bolletii; and two sub-clusters in clusters C2 and C3. The phylogenomic network confirms these three clusters. The genome length (from 4.8 to 5.51-Mb) varies from 5.07-Mb in C1, 4.89-Mb in C2A, 5.01-Mb in C2B and 5.28-Mb in C3. The mean number of prophage regions (from 0 to 7) is 2 in C1; 1.33 in C2A; 3.5 in C2B and five in C3. A total of 36 genes are uniquely present in C1, 15 in C2 and 15 in C3. These genes could be used for the detection and identification of organisms in each cluster. Further, the mean number of host-interaction factors (including PE, PPE, LpqH, MCE, Yrbe and type VII secretion system ESX3 and ESX4) varies from 70 in cluster C1, 80 in cluster C2A, 74 in cluster C2B and 93 in clusters C3A and C3B. No significant differences in antibiotic resistance genes were observed between clusters, in contrast to previously reported in-vitro patterns of drug resistance. They encode both penicillin-binding proteins targeted by β-lactam antibiotics and an Ambler class A β-lactamase for which inhibitors exist.
Our comparative analysis indicates that M. abscessus complex comprises three genomospecies, corresponding to M. abscessus, M. bolletii, and M. massiliense. The genomics data here reported indicate differences in virulence of medical interest; and suggest targets for the refined detection and identification of M. abscessus.
KeywordsMycobacterium abscessus Mycobacterium bolletii Mycobacterium massiliense Araucaria Mycobacteriophage Prophage
The non-tuberculous mycobacterium Mycobacterium abscessus was long confused with Mycobacterium chelonae. Other closely related species include Mycobacterium salmoniphilum, Mycobacterium immunogenum, Mycobacterium massiliense, Mycobacterium bolletii and Mycobacterium franklinii altogether forming the Mycobacterium chelonae-abscessus complex. This complex is the third most frequent mycobacterial complex infecting humans in developed countries besides the Mycobacterium tuberculosis and Mycobacterium avium complexes [7, 8]. Bibliometrics retrieving over 1,700 publications in the Medline database illustrates the fact that this complex is emerging, causing both sporadic cases and outbreaks of community-acquired and health-care associated infections . Not only humans but also cats [10, 11] and dolphins [12–14] are infected while fishes are uniquely infected by M. salmoniphilum[2, 15].
Current nomenclature is that the species M. abscessus comprises two subspecies named M. abscessus subsp. abscessus and M. abscessus subsp. bolletii. Later taxon accommodates isolates previously referred as M. bolletii or M. massiliense. This nomenclature however may obscure the true diversity of mycobacteria in this complex. While the 16S rRNA gene yields an identical sequence for M. abscessus and M. bolletii, it shares 99% sequence identity with M. massiliense. RpoB gene sequencing founded the description of recent species [17–19] but yielded further conflicting results [20–22]. Multilocus sequencing analysis  and multispacer sequence typing  differentiated M. massiliense from M. bolletii. In this report, the previous nomenclature M. abscessus, M. bolletii and M. massiliense forming the M. abscessus complex, has been retained for clarity.
List of Mycobacterium abscessus genomes here studied
M. abscessus Type strain
human knee infection
M. abscessus M93
sputum sample from a Malaysian patient presenting with a prolonged productive cough suggestive of a bacterial lower respiratory tract infection
M. abscessus M94
sputum sample of a Malaysian patient with a persistent cough and fever and consolidation in the chest radiograph
M. abscessus M152
acid-fast bacillus positive sputum of a Malaysian man
M. massiliense strain GO 06
undergone knee joint surgery
M. massiliense Type strain
sputum specimen from hemoptoic pneumonia
M. massiliense M18
lymph node biopsy specimen from a Malaysian patient suspected of having tuberculous cervical lymphadenitis
M. massiliense M154
bronchoalveolar lavage fluid of a Malaysian patient presenting with lower respiratory tract infection
M. abscessus 47 J26
sputum sample from a patient with Cystis fibrosis
M. abscessus M115
sputum from a Malaysian patient presenting with persistent cough and loss of body weight suggestive of pulmonary tuberculosis
M. abscessus M139
sputum sample of a 26-year-old Nepalese male presenting with hemoptysis
M. abscessus M172
putum isolate from a Malaysian patient
M. bolletii Type strain
respiratory tract specimen collected in woman with hemoptoic pneumonia
M. abscessus M24
the bronchoalveolar lavage fluid of a Malaysian patient
Results and discussion
M. abscessuscomplex pan- and core-genome
Mycobacterium abscessus core genome and unique genes
Unique core genome
M. abscessus T
strain GO 06
M. massiliense T
M. bolletii T
M. abscessus core genome
M. abscessuscomplex diversity
Average nucleodite identity and characteristics of Mycobacterium abscessus genomes
Genome lenght Mb
AAI Vs M. abscessusT
AAI Vs M. bolletiiT
AAI Vs massilienseT
M. abscessus T
strain GO 06
M. massiliense T
M. bolletii T
C1 strains have been isolated from American and Malaysian patients suffering knee infection and lower respiratory infection, respectively (Table 1). C2A strains were isolated from Malaysian and French patients suffering severe, respiratory tract infections. C2B strains were isolated from Nepalese, Malaysian and English patients suffering respiratory tract infections, including cystis fibrosis and pulmonary tuberculosis patients. C3A and C3B strains were exclusively isolated from patients suffering respiratory tract infections, in France and Malaysia, respectively. Therefore, clusters specify the clinical form and geographical origin of the infection.
Altogether, genomics analyses revealed a more heterogeneous structure of M. abscessus complex than the one currently suggested by the nomenclature, which recognizes only two subspecies within M. abscessus. It has been proposed that two genomes exhibiting AAI >96% belong to the same species [34, 35]. Therefore, AAI analysis indicates that M. abscessus is in fact comprising of three genomospecies, corresponding to previous nomenclature of M. abscessus (C1), M. massiliense (C2) and M. bolletii (C3). Using an AAI <97% threshold would further determine two subspecies in M. massiliense (C2A and C2B) and in M. bolletii (C3A and C3B). Recent whole genome sequencing analyses of clinical isolates in Great Britain also clearly distinguished three clusters in agreement with the three here reported . All these data support revaluating the taxonomy of M. abscessus complex, to recognize three genomospecies M. abscessus (C1), M. bolletii (C2), and M. massiliense (C3); and four unnamed subspecies C2A, C2B; C3A, C3B.
M. abscessus median GC% content is 64.2%, ranging from 62.7% (M. abscessus ATCC 19977) to 64.2% (strain Go 06). The GC% is not characteristic of the clusters as the median GC% content of C1, C2A and C3 is 64.2%, close to the median 64.1% GC% content in C2B.
Mycobacterium abscessus prophages
M. abscessus T
M. massiliense T
M. bolletii T
M. abscessuscomplex resistome
As all mycobacteria, M. abscessus complex is embedded into a hydrophobic cell wall barrier to hydrophilic antibiotics. Accordingly, M. abscessus is multidrug resistant organisms exhibiting different drug resistance [42–44]. M. abscessus genomes encode many proteins potentially involved in drug-efflux systems, including members of the major facilitator family, ABC transporters and MmpL proteins; Small Multidrug Resistance-family, a family of lipophilic drug efflux proteins ; and a multidrug resistance stp protein similar to M. tuberculosis involved in spectinomycin and tetracycline resistance . M. abscessus, M. bolletii and M. massiliense were reported to be in-vitro susceptible to amikacin; however, comparison with the M. tuberculosis H37Rv resistome and the antibiotic resistance databases indicate that M. abscessus encodes an aminoglycoside 29-N-acetyltransferase and aminoglycoside phosphotransferases involved in resistance to aminoglycosides. Also, genetic analyses disclosed 16S rRNA gene mutations conferring aminoglycoside resistance [4, 5, 47]. Indeed, the presence of a single rRNA operon in all of the M. abscessus genomes favours the occurrence of dominant mutations conferring resistance to aminoglycosides and macrolides. M. abscessus genomes encode a rifampin ADP-ribosyl transferase and monooxygenases potentially involved in resistance to rifampin and tetracyclines. Moreover, M. abscessus genomes encode three tet(M) genes conferring resistance to tetracyclyine and doxycycline; the number of tet(M) genes was correlated to the resistance to cyclines in Escherichia coli. However, M. massiliense was reported to be susceptible and M. abscessus and M. bolletii to be resistant to doxycycline . M. abscessus genomes encode resistance to fusidic acid, glycopeptides, MLS (Macrolide-Lincosamide-StreptograminB), phenicols, rifampicin, sulphonamide and trimethoprim. Also, M. abscessus genomes encode FolP homologs conferring resistance to cotrimoxazole, homolog of UDP-N- acetylglucosamine 1-carboxyvinyltransferase, a MurA protein conferring resistance to fosfomycin and homologs of 23S rRNA methylases conferring resistance to macrolides. Also, M. abscessus genome encodes an erm(41) gene which mutations were reported to confer clarithromycin resistance . In-vitro tests showed that M. massiliense clinical isolates could be distinguished from M. abscessus isolates for their susceptibility to ciprofloxacin  whereas M. bolletii isolates were reported to be resistant to all quinolones . A mutation at codon 90 in gyrA gene was reported in clinical isolates of M. abscessus exhibiting high resistance to ciprofloxacin . This observation contrasts with our genome analysis, which found no such mutations, suggesting that other mechanisms of resistance may be involved in high-level resistance to quinolones . Accordingly, we found that M. abscessus mycobacteria encode qepA2, a plasmidic gene conferring quinolone resistance in gram-negative bacteria . M. abscessus mycobacteria were reported to be in-vitro resistant to penicillin, amoxicillin, cefoxitin, ceftriaxone, cefotaxime and imipenen [4, 5]. This contrasts with the fact that they encode Penicillin-binding proteins (PBPs), targets for β-lactam antibiotics (except for tabtoxinine-β-lactam, which inhibits glutamine synthetase), which are essential for peptidoglycan synthesis [54, 55]. M. abscessus genomes encode an Ambler class A β-lactamase homologous to β-lactamases in gram-negative bacteria and to two β-lactamases in M. tuberculosis. β-lactamases inhibitors have not been evaluated against M. abscessus sensu lato mycobacteria.
Genome-based analysis of host-interactions
Our in-depth genomic analyses indicate that M. abscessus has a non-conservative genome, suggesting the possibility of on-going transfer of additional genetic material. Unsurprisingly, M. abscessus has already acquired antibiotic resistance. Also, phages have mediated diversity and horizontal gene transfer which drived the rapid evolution of this complex. Indeed, gene transfers have driven the evolution of M. abscessus towards three different genomospecies M. abscessus, M. massiliense and M. bolletii; and the evolution of four different yet unnamed subspecies. Each genomospecies has its own specificities in terms of genome size, prophagome and genome content. We identified 66 genes uniquely present in each genomospecies; these genes could be used in refined detection and identification of M. abscessus organisms. These genomic differences support differences in host interactions and the clinical presentation of infection with M. massiliense (C2A and C2B) being more virulent than the two other genomospecies. Host-interaction factors may contribute to the ability of M. abscessus to colonize mammalian hosts where its respiratory tract habitat put it in close proximity to other serious opportunist pathogens which can act as donors of additional host-interaction factors.
Here reported informations regarding differences between M. abscessus genomespecies will help understanding their pathogenesis factors and could reveal new, more specific targets for drug design and diagnosis tools.
The whole genomes of 14 M. abscessus strains were downloaded from Genbank (Table 1). The genomic sequence, either contigs or finished genomes were concatenated to one pseudogenome per genome.
Prophage detection and genome annotation
Protein sequences were predicted using prodigal software  to generate normalized files containing the combined protein sequences of all 14 genomes. Prophage regions were detected using PHAST software (Table 4). Predicted proteins were annotated using BLASTp against the National Center for Biotechnology Information (NCBI) non-redundant (NR) database, UNIPROT (http://www.uniprot.org/), the Clusters of Orthologous Groups (COG)  and a home-made antibiotic resistance gene database.
Genome clustering and calculation of core genomes
Proteome sequences were compared using by BlastP and pairwise alignments using ClustalW and the ANI was determined by the mean percentage of nucleotide sequence identity of core proteins . We clustered the M. abscessus homologous genes using orthoMCL  on the translated protein sequences of all predicted genes with a conservative parameter value of 50% sequence identity. The determination of the different unique core genomes was based on the homology clusters found by orthoMCL.
M. abscessus proteomes were aligned using Mauve software  to infer phylogeny using the Neighbor-Net algorithm in the package SplitsTree4 . The orthologous group data found by orthoMCL were used to construct a whole-genome phylogenetic tree based on gene content. We generated a matrix of binary discrete characters (“0” and “1” for absence and presence, respectively) . Using this matrix, we constructed a phylogenetic tree implementing the neighbor-joining (NJ) method within SplitsTree4 .
Availability of supporting data
The data set of Figure 1C supporting the results of this article is available in the TreeBase (http://treebase.org/treebase-web/home.html) repository, under the accession URL http://purl.org/phylo/treebase/phylows/study/TB2:S15632.
MS is financially supported by the Infectiopôle Sud Foundation.
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