Mycobacterium tuberculosis colonies in culture, from the Center for Disease Control and Prevention.

Belongs within: Corynebacteriales.

Mycobacterium is a genus of aerobic to mesophilic bacteria producing high concentrations of mycolic acids.

Life in mycolates
Published 16 January 2008
Mycobacterium tuberculosis, from here.

Among the best-known genera of bacteria is unquestionably Mycobacterium. The most famous members of this genus, of course, are the human pathogens Mycobacterium tuberculosis (the cause of, well, tuberculosis) and M. leprae (causing leprosy). Back home in New Zealand, though, the most significant species is possibly M. bovis, which causes bovine tuberculosis, and a whole host of other species infect various other mammals and birds. Mycobacterium also includes a number of non-pathogenic forms such as M. smegmatis. In culture, mycobacteria are clearly divisible into fast-growing and slow-growing taxa. Phylogenetic analyses suggest that the slow-growing taxa (which include the major pathogens) may form a single clade (Devulder et al. 2005).

Mycobacterium leprae is a very strange organism, even if we leave aside its apparent ability to survive on only two host species, humans and armadillos. As prominent human pathogens, M. tuberculosis and M. leprae have both been subject to genome-sequencing projects. The differences between the two species can only be described as remarkable. Bacterial genomes tend to be fairly streamlined things, probably because the rapid generation times and hence rapid evolutionary rates mean that non-functional genetic elements would soon be pruned from the genome. The genome of M. tuberculosis is no exception. ~91% of the genome is made up of protein-coding sequences, with only six pseudogenes (Cole et al. 1998). That of M. leprae, however, is an entirely different affair (Cole et al. 2001). Not only is it much smaller than that of M. tuberculosis (~3000 ORFs* in M. leprae as opposed to ~4000 in M. tuberculosis) but it also contains a much higher proportion of junk. Less than half of the genome appears functional, with a whopping 1116 pseudogenes. Even those genes that retain the appearance of functionality may not actually be so—comparative proteome analysis recovered only 391 soluble protein species in M. leprae, as opposed to ~1800 in M. tuberculosis.

*ORF—Open Reading Frame. An ORF is a section of the genome that has characteristics suggesting that it might be a functional gene (such as an copy initiation site) but may or may not have been definitely connected to a functional product.

From Cole et al. (2001): (a) diagram of the prolyl-tRNA synthetase gene (proS) regions in the genomes of Mycobacterium leprae (above) and M. tuberculosis (below). Arrows represent genes or operons, crosses indicate pseudogenes. Note the different positions of proS in the two species. (b) Domain structures of the proteins of the two species. Note the significantly different structure of the M. leprae synthetase, which may have been acquired through horizontal gene transfer from the eukaryote host.

It is not hard to imagine how this situation arose. Many obligately parasitic organisms such as Mycobacterium leprae show reduction in functionality—why invest time and energy into producing something yourself when your host provides it ready-made? Leprosy (and hence probably the organism that causes it) may have originated quite recently. Palaeopathological evidence does not indicate its presence prior to the development of urbanisation, and it is difficult to imagine how M. leprae, with its combination of obligate parasitism yet extremely low communicability, could have maintained a viable population without a dense host population (Pinhasi et al. 2006). It seems that with M. leprae we might be seeing reduction in action—the non-vital factors have lost their function, but their remnants have not yet been purged from the genome*.

*It occurs to me that my wording in describing the loss of non-functional elements from bacterial genomes makes it sound like an active process—as if some factor in the organism’s metabolism was directly seeking out and removing unneeded pieces of DNA. This is not necessarily the case. Even if the loss of pseudogenes and such was completely random, there would probably still be a tendency for populations to lose them over time, as bacteria with smaller genomes but no loss of viability would probably have a selective advantage over those with larger genomes because they would be able to grow and replicate faster.

Mycobacterium smegmatis growing as a film on water, from ScienceDaily.

As regards the non-pathogenic mycobacteria, probably the best known is the aforementioned Mycobacterium smegmatis. This species is generally a soil bacterium, though it can cause opportunistic infections (generally in patients already suffering from immuno-suppression)—the name “smegmatis” refers to its initial isolation from human genital secretions. Because M. smegmatis, as a fast-growing Mycobacterium, is far easier to culture than the slow-growing pathogenic species, is has become widely used as a model organism in the study of mycobacteria.

Systematics of Mycobacterium

Characters (from Nouioui et al. 2018): aerobic to mesophilic, Gram-stain-positive, acid-fast, non-motile, asporogenous, usually forming slightly curved or straight rods, occasionally branched filaments. Peptidoglycan of A1α type. Muramic acid residues of peptidoglycan N-glycolated. Whole-cell hydrolysates containing DL-A2pm, arabinose and galactose. Predominant isoprenologue MK-9(H2), major polar lipids are DPG, PE, PI, and PIMs, main fatty acids straight-chain saturated, unsaturated and 10-methyloctadecanoic (tuberculostearic) acids. Mycolic acids with 60–90 carbon atoms; fatty acid esters released on pyrolysis mass spectrometry (MS) of mycolic acid esters with 22–26 carbon atoms. G+C content around 55–75%.

    |  i. s.: M. bovisAC03
    |         M. farcinogenesNC18
    |         M. globerulumK-WK92
    |         M. lepraePHK96
    |         M. lutetienseNC18
    |         M. malmoenseNC18
    |         M. porcinumNC18
    |         M. senegalenseNC18
    |--+--+--M. saopaulenseNC18
    |  |  `--+--M. chelonae Bergey et al. 1923NC18
    |  |     `--M. salmoniphilum (ex Ross 1960) Whipps et al. 2007NC18
    |  `--+--M. abscessusNC18
    |     |    |--M. a. ssp. abscessusNC18
    |     |    |--M. a. ssp. bolletii (Adékambi et al. 2006) Leao et al. 2011NC18
    |     |    `--M. a. ssp. massiliense (Adékambi et al. 2006) Tortoli et al. 2016NC18
    |     `--+--M. franklinii Nogueira et al. 2015NC18
    |        `--M. immunogenum Wilson et al. 2001NC18
    `--+--+--M. aubagnenseNC18
       |  `--+--M. mucogenicumNC18
       |     `--M. phocaicumNC18
       `--+--+--+--M. insubricumNC18
          |  |  `--+--M. fallax Lévy-Frébault et al. 1983NC18
          |  |     `--+--M. chitaeNC18
          |  |        `--M. confluentis Kirschner et al. 1992NC18
          |  `--+--+--M. helvumNC18
          |     |  `--+--M. aichienseNC18
          |     |     `--+--M. aromaticivorans Hennessee et al. 2009NC18
          |     |        `--M. rhodesiae (ex Tsukamura et al. 1971) Tsukamura 1981NC18
          |     `--+--+--+--+--M. oryzaeNC18
          |        |  |  |  `--+--M. muraleNC18
          |        |  |  |     `--M. tokaienseNC18
          |        |  |  `--+--M. brisbanenseNC18
          |        |  |     |--+--M. bacteremicumNC18
          |        |  |     |  `--M. neoaurumNC18
          |        |  |     `--+--M. cosmeticum Cooksey et al. 2004NC18
          |        |  |        `--+--M. canariasenseNC18
          |        |  |           `--+--M. diemhoferiNC18
          |        |  |              `--+--M. fluoranthenivoransNC18
          |        |  |                 `--M. frederiksburgenseNC18
          |        |  `--+--+--+--M. goodiiNC18
          |        |     |  |  `--M. smegmatis (Trevisan 1889) Lehmann & Neumann 1899NC18
          |        |     |  `--+--M. madagascarienseNC18
          |        |     |     `--+--M. hodleriNC18
          |        |     |        `--+--M. arabienseNC18
          |        |     |           `--M. sediminisNC18
          |        |     `--+--+--M. mageritense Domenech et al. 1997NC18
          |        |        |  `--M. wolinskyi Brown et al. 1999NC18
          |        |        `--+--M. houstonense Schinsky et al. 2004NC18
          |        |           `--+--M. setense Lamy et al. 2008NC18
          |        |              `--+--+--M. neworleansense Schinsky et al. 2004NC18
          |        |                 |  `--M. septicum Schinsky et al. 2000NC18
          |        |                 `--+--+--M. boenickei Schinsky et al. 2004NC18
          |        |                    |  `--M. conceptionense Adékambi et al. 2006NC18
          |        |                    `--+--M. fortuitum da Costa Cruz 1938NC18
          |        |                       |    |--M. f. ssp. fortuitumNC18
          |        |                       |    `--M. f. ssp. acetamidolyticumNC18
          |        |                       `--+--M. peregrinum (ex Bojalil et al. 1962) Kusunoki & Ezaki 1992NC18
          |        |                          `--+--M. alveiNC18
          |        |                             |--M. arcueilenseNC18
          |        |                             `--+--M. llatzerenseNC18
          |        |                                `--M. montmartrenseNC18
          |        `--+--+--+--M. obuense (ex Tsukamura & Mizuno 1971) Tsukamura & Mizuno 1981NC18
          |           |  |  `--+--M. psychrotoleransNC18
          |           |  |     `--+--M. poriferaeNC18
          |           |  |        `--+--M. rufum Hennessee et al. 2009NC18
          |           |  |           `--+--M. chlorophenolicum (Apajalahti et al. 1986) Häggblom et al. 1994NC18
          |           |  |              `--M. chubuense (ex Tsukamura 1973) Tsukamura 1981NC18
          |           |  `--+--+--M. parafortuitumNC18
          |           |     |  `--+--M. vaccae Bönicke & Juhasz 1964NC18
          |           |     |     `--+--M. austroafricanum Tsukamura et al. 1983NC18
          |           |     |        `--M. vanbaalenii Khan et al. 2002NC18
          |           |     `--+--M. iranicum Shojaei et al. 2013NC18
          |           |        `--+--M. gilvumNC18
          |           |           `--+--M. sarraceniaeNC18
          |           |              `--+--M. aurum Tsukamura 1966NC18
          |           |                 `--M. pyrenivoransNC18
          |           `--+--M. tusciaeNC18
          |              `--+--M. anyangenseNC18
          |                 |--+--M. agriNC18
          |                 |  `--M. duvaliiNC18
          |                 `--+--+--M. doricum Tortoli et al. 2001NC18
          |                    |  `--M. monacense Reischl et al. 2006NC18
          |                    `--+--+--M. hippocampiNC18
          |                       |  `--M. novocastrenseNC18
          |                       `--+--M. thermoresistibile Tsukamura 1966NC18
          |                          `--+--M. hassiacum Schröder et al. 1997NC18
          |                             `--+--M. moriokaense Tsukamura et al. 1986NC18
          |                                `--+--M. phlei Lehmann & Neumann 1899NC18
          |                                   |--+--M. elephantisNC18
          |                                   |  `--M. pulverisNC18
          |                                   `--+--M. brumaeNC18
          |                                      |--+--M. celeriflavum Shahraki et al. 2015NC18
          |                                      |  `--M. malmesburyenseNC18
          |                                      `--+--M. flavescensNC18
          |                                         `--M. rutilum Hennessee et al. 2009NC18
          `--+--M. pallensNC18
             |--+--M. crocinumNC18
             |  `--+--M. komossenseNC18
             |     `--M. sphagniNC18
             `--+--+--+--M. trivialeNC18
                |  |  `--+--M. koreense Kim et al. 2012NC18
                |  |     `--M. parakoreenseNC18
                |  `--+--+--+--M. algericum Sahraoui et al. 2011NC18
                |     |  |  `--M. senuense Mun et al. 2008NC18
                |     |  `--+--M. kumomotonense Masaki et al. 2007NC18
                |     |     `--M. terraeNC18
                |     `--+--M. longobardum Tortoli et al. 2013NC18
                |        `--+--M. paraterraeNC18
                |           `--+--M. heraklionenseNC18
                |              `--+--+--M. arupense Cloud et al. 2006NC18
                |                 |  `--M. minnesotense Hannigan et al. 2013NC18
                |                 `--+--M. nonchromogenicumNC18
                |                    `--+--M. engbaekii Tortoli et al. 2013NC18
                |                       `--M. hiberniae Kazda et al. 1993NC18
                `--+--M. holsaticumNC18
                   `--+--+--+--M. noviomagense van Ingen et al. 2009NC18
                      |  |  `--+--M. heckeshornense Roth et al. 2001NC18, JC08
                      |  |     `--+--M. botnienseNC18
                      |  |        `--M. xenopi Schwabacher 1959NC18
                      |  `--+--M. fragae Ramos et al. 2013NC18
                      |     `--+--M. shimoidei (ex Tsukamura et al. 1975) Tsukamura 1982NC18
                      |        `--+--M. cookiiNC18
                      |           `--+--M. celatum Butler et al. 1993NC18
                      |              `--+--M. branderi Koukila-Kähkölä et al. 1995NC18
                      |                 `--M. kyorinense Okazaki et al. 2009NC18
                      `--+--+--M. haemophilum Sompolinsky et al. 1978NC18
                         |  `--+--+--+--M. bourgelatiiNC18
                         |     |  |  `--M. intermedium Meier et al. 1993NC18
                         |     |  `--+--M. kubicae Floyd et al. 2000NC18
                         |     |     `--+--M. asiaticum Weiszfeiler et al. 1971NC18
                         |     |        `--+--M. gordonae Bojalil et al. 1962NC18, AS92
                         |     |           `--M. paragordonaeNC18
                         |     `--+--+--M. marinumNC18
                         |        |  |--M. pseudoshottsii Rhodes et al. 2005NC18
                         |        |  |--M. shottsiiNC18
                         |        |  |--M. ulceransNC18
                         |        |  `--+--M. gastriNC18
                         |        |     `--M. kansasii Hauduroy 1955NC18
                         |        `--+--+--M. lacus Turenne et al. 2002NC18
                         |           |  `--+--M. riyadhense van Ingen et al. 2009NC18
                         |           |     `--+--M. angelicumN18
                         |           |        `--M. szulgai Marks et al. 1972NC18
                         |           `--+--M. shinjukuense Saito et al. 2011NC18
                         |              `--+--*M. tuberculosisNC18
                         |                 |--M. africanumNC18
                         |                 |--M. caprae (Aranaz, Liébana et al.) Aranaz, Cousins et al. 2003NC18, AC03 (see below for synonymy)
                         |                 |--M. microtiNC18
                         |                 `--M. pinnipediiNC18
                         `--+--M. conspicuum Springer et al. 1996NC18
                            `--+--+--+--M. sherrisii van Ingen et al. 2011NC18
                               |  |  `--+--M. lentiflavumNC18
                               |  |     `--M. simiae Karassova et al. 1965NC18
                               |  `--+--+--M. florentinum Tortoli et al. 2005NC18
                               |     |  `--M. stomatepiaeNC18
                               |     `--+--M. genavense Böttger et al. 1993NC18
                               |        |--M. monteforiense Levi, Bartell et al. 2003VP NC18, IJSEM03
                               |        `--M. triplex Floyd et al. 1997NC18
                               `--+--+--+--M. bohemicum Reischl et al. 1998NC18
                                  |  |  `--M. saskatchewanense Turenne et al. 2004NC18
                                  |  `--+--+--M. heidelbergense Haas et al. 1998NC18
                                  |     |  `--M. palustre Torkko et al. 2002NC18
                                  |     `--+--M. alsense Tortoli et al. 2016NC18
                                  |        `--+--M. interjectum Springer et al. 1995NC18
                                  |           `--M. paraense da Costa et al. 2015NC18
                                  `--+--+--M. parmense Fanti et al. 2004NC18
                                     |  `--+--M. nebraskense Mohamed et al. 2004NC18
                                     |     `--+--+--M. europaeum Tortoli et al. 2011NC18
                                     |        |  `--+--M. paraseoulense Lee et al. 2010NC18
                                     |        |     `--M. seoulenseNC18
                                     |        `--+--M. parascrofulaceum Turenne et al. 2004NC18
                                     |           `--+--M. paraffinicumNC18
                                     |              `--M. scrofulaceum Prissick & Masson 1956NC18
                                     `--+--+--M. arosiense Bang et al. 2008NC18
                                        |  |--M. timonenseNC18
                                        |  `--+--M. mantenii van Ingen et al. 2009NC18
                                        |     `--+--M. colombiense Murcia et al. 2006NC18
                                        |        `--M. vulneris van Ingen et al. 2009NC18
                                        `--+--M. avium [incl. M. bouchedurhonense Ben Salah et al. 2009]NC18
                                           |    |--M. a. ssp. aviumNC18
                                           |    |--M. a. ssp. paratuberculosisNC18
                                           |    `--M. a. ssp. silvaticumNC18
                                           `--+--M. marseillense Ben Salah et al. 2009NC18
                                              `--+--M. intracellulareNC18
                                                 |    |--M. i. ssp. intracellulareNC18
                                                 |    |--M. i. ssp. chimaera (Tortoli et al.) Nouioui, Carro et al. 2018 (see below for synonymy)NC18
                                                 |    `--M. i. ssp. yongonense (Kim et al.) Nouioui, Carro et al. 2018 (see below for synonymy)NC18
                                                 `--M. paraintracellulare Lee et al. 2016NC18

Mycobacterium caprae (Aranaz, Liébana et al.) Aranaz, Cousins et al. 2003NC18, AC03 [=M. tuberculosis ssp. caprae Aranaz, Liébana et al. 1999AC03, M. bovis ssp. caprae (Aranaz et al.) Niemann et al. 2002AC03]

Mycobacterium intracellulare ssp. chimaera (Tortoli et al.) Nouioui, Carro et al. 2018 [=M. chimaera Tortoli et al. 2004]NC18

Mycobacterium intracellulare ssp. yongonense (Kim et al.) Nouioui, Carro et al. 2018 [=M. yongonense Kim et al. 2013]NC18

*Type species of generic name indicated


[AS92] Aragno, M., & H. G. Schlegel. 1992. The mesophilic hydrogen-oxidizing (knallgas) bacteria. In: Balows, A., H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer (eds) The Prokaryotes: A handbook on the biology of bacteria: Ecophysiology, isolation, identification, applications 2nd ed. vol. 1 pp. 344–384. Springer-Verlag: New York.

[AC03] Aranaz, A., D. Cousins, A. Mateos & L. Domínguez. 2003. Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov. International Journal of Systematic and Evolutionary Microbiology 53: 1785–1789.

Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry, III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M.-A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead & B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 (6685): 537–544.

Cole, S. T., K. Eiglmeier, J. Parkhill, K. D. James, N. R. Thomson, P. R. Wheeler, N. Honoré, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M. A. Quail, M.-A. Rajandream, K. M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J. R. Woodward & B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409 (6823): 1007–1011.

Devulder, G., M. Pérouse de Montclos & J. P. Flandrois. 2005. A multigene approach to phylogenetic analysis using the genus Mycobacterium as a model. International Journal of Systematic and Evolutionary Microbiology 55: 293–302.

[IJSEM03] IJSEM. 2003. Validation list no. 94. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. International Journal of Systematic and Evolutionary Microbiology 53: 1701–1702.

[JC08] Judicial Commission of the International Committee on Systematics of Prokaryotes. 2008. Status of strains that contravene Rules 27 (3) and 30 of the International Code of Nomenclature of Bacteria. Opinion 81. International Journal of Systematic and Evolutionary Microbiology 58: 1755–1763.

[K-WK92] Korn-Wendisch, F., & H. J. Kutzner. 1992. The family Streptomycetaceae. In: Balows, A., H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer (eds) The Prokaryotes: A handbook on the biology of bacteria: Ecophysiology, isolation, identification, applications 2nd ed. vol. 1 pp. 921–995. Springer-Verlag: New York.

[NC18] Nouioui, I., L. Carro, M. García-López, J. P. Meier-Kolthoff, T. Woyke, N. Kyrpides, C., R. Pukall, H.-P. Klenk, M. Goodfellow & M. Göker. 2018. Genome-based taxonomic classification of the phylum Actinobacteria. Frontiers in Microbiology 9: 2007.

Pinhasi, R., R. Foley & H. D. Donoghue. 2006. Letter: Reconsidering the antiquity of leprosy. Science 312 (5775): 846.

[PHK96] Prescott, L. M., J. P. Harley & D. A. Klein. 1996. Microbiology 3rd ed. Wm. C. Brown Publishers: Dubuque (Iowa).

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