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MINIREVIEW

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Mycobacterial Taxonomy
Betty A. Forbes
Department of Pathology, Virginia Commonwealth University Medical Center, Richmond, Virginia, USA

ABSTRACT This article summarizes the most recent (since 2012) taxonomic changes
in the genus Mycobacterium. Only those mycobacteria that have been isolated from Accepted manuscript posted online 7
December 2016
human specimens are included in this summary.
Citation Forbes BA. 2017. Mycobacterial
KEYWORDS human specimens, mycobacteria, taxonomy taxonomy. J Clin Microbiol 55:380 –383. https://
doi.org/10.1128/JCM.01287-16.
Editor Colleen Suzanne Kraft, Emory University

C urrently, there are over 170 recognized species of Mycobacterium, the only genus
in the family Mycobacteriaceae. Organisms belonging to this genus are quite
diverse with respect to their ability to cause disease in humans; some are strict
Copyright © 2017 American Society for
Microbiology. All Rights Reserved.
Address correspondence to baforbes@vcu.edu.

pathogens, while others are opportunistic pathogens or nonpathogenic. Similar to


other major groups of bacteria, the mycobacteria have undergone an extraordinary
expansion in the number of different species over the last 2 decades, due in large part
to the discriminatory power of gene sequencing, which phenotypic methods cannot
achieve. This discriminatory power is such that phenotypic traits, i.e., biochemical and
cultural characteristics, are no longer acceptable for the identification of mycobacteria.
Paralleling the increasing number of mycobacterial species, infections caused by the
nontuberculous mycobacteria (NTM), in particular, are also increasing on a worldwide
level (1). For laboratories identifying mycobacteria isolated from clinical specimens, it is
essential that these organisms are accurately identified for proper clinical management.
As more clinical laboratories use molecular or other methods, such as mass spectrom-
etry, for identification, our understanding of clinical significance will change and evolve
as the number of case reports regarding the “new” species increase; it may well be that

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the role of many of the newly described mycobacterial species has been underesti-
mated either because of misidentification or because the species were unrecognized.
Toward this end, it is imperative for clinical microbiologists to keep up to date with the
rapidly evolving taxonomy of the mycobacteria. The intent of this minireview is to
provide a single reference for diagnostic laboratories regarding new, clinically relevant
changes in taxonomy pertaining to the genus Mycobacterium.

METHODS
Only those newly recognized mycobacterial species recovered from human clinical
material and reported between January 2012 and December 2015 are summarized
here. These new species were identified using a combination of reference materials. A
valuable resource was the List of Prokaryotic Names with Standing in Nomenclature
(http://www.bacterio.net/-allnamesmr.html). In addition, a combination of reference
materials was used, including the Manual of Clinical Microbiology, 11th edition, chapters
30 through 32; the International Journal of Systematic and Evolutionary Microbiology;
and the PubMed database (http://www.ncbi.nlm.nih.gov/pubmed), using “nov. sp.
Mycobacterium” as the search term.

RESULTS
Table 1 summarizes new Mycobacterium species identified between January 2012
and December 2015. For each species, the human source(s) from which the new species
was isolated, its clinical relevance, and noteworthy growth characteristics are noted. In
addition, information on whether 16S rRNA gene sequencing identified the species is

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Minireview Journal of Clinical Microbiology

TABLE 1 New mycobacterial species (family: Mycobacteriaceae) recovered between January 2012 and December 2015
Unique 16S
rRNA gene? If
not, gene
Scientific name (year sequence
identified) Sourcea Clinical relevance Growth characteristics alternative References
M. alsense (2015) Sputum Infection Slow grower; weak yellow pigment Yes 2, 3
on Lowenstein Jensen medium,
not Middlebrook 7H11; most
closely related to M. szulgai and
M. malmoense
M. celeriflavum (2015) Sputum Undetermined; colonizer Rapid grower; scotochromogen Yes 1, 4
(rough, pale yellow); most
closely related to M. flavescens
and M. novocastrense
M. engbaekii (2013) Urine, gastric wash fluid, Undetermined; colonizer Slow grower; most closely related Yes 1, 5
bronchial aspirate to M. terrae complex (namely, M.
hiberniae); pigmented (some
show pink photochromogenic
pigmentation)
M. fragae (2013) Sputum Undetermined; colonizer Slow grower; smooth colonies, Yes 1, 6
unpigmented; closely related to
M. celatum
“M. franklinii”b (2015) Respiratory tract, skin, Infection; colonizer Rapid grower; nonpigmented; No; rpoB, hsp65 1, 7, 8
granulomatous liver closely related to M.
lesion, central line chelonae/abscessus
infection
“M. fukienense”b (2013) Respiratory tract Undetermined; colonizer Rapid grower; nonpigmented; No; hsp65 1, 9
closely related to M.
chelonae/abscessus
M. heraklionense (2013) Respiratory: BAL and Undetermined; colonizer Slow grower; nonpigmented; Yes 1,5
sputum closely related to M. terrae
complex, namely, to M.
arupense; optimal growth temp
25–37°C
M. iranicum (2013) Sputum, BAL, CSF, hand Infection; colonizer Rapid grower; scotochromogen; Yes 1,10–14
wound, peritoneal closely related to M. gilvum
fluid
M. koreense (2012) Sputum Undetermined Slow grower; nonpigmented; Yes 1,15

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closely related to M. triviale
M. longobardum (2013) Sputum, bone Respiratory, colonizer; Slow grower; most closely related Yes 1,5,16
osteomyelitis to M. terrae complex
M. paragordonae Sputum Undetermined Slow grower; scotochromogen; Yes 1,17
(2014) closely related to M. gordonae
M. parakoreense (2013) Sputum Undetermined Slow grower; yellow or Yes 1,18
nonpigmented; closely related to
M. koreense
M. yongonense (2013) Sputum, BAL, stool Infection; colonizer Slow grower; nonpigmented; No; hsp65 1,19,20
closely related to M.
intracellulare
aBAL, bronchoalveolar lavage fluid; CSF, cerebrospinal fluid.
bCurrently a nonvalidated species.

included. In addition, brief summaries of case reports for some of the new species are
provided in Table 2.

DISCUSSION
Accurate identification of the mycobacteria is a challenge, particularly in light of the
extraordinary number of species in the genus. It has become clear that identification of
mycobacteria based on phenotypic and culture traits is poorly reproducible, time
consuming, and lacking in sufficient discriminatory power (21). As a result, this ap-
proach to mycobacterial identification has been abandoned for the most part. Al-
though the introduction of numerous new species over recent years might seem
daunting to clinical laboratories that identify mycobacteria, accurate identification is

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TABLE 2 Brief summaries of clinical case reports for new Mycobacterium species
Organism Infections Reference
M. alsense Bronchopneumonia in two 70-yr-old subjects; both responded to antimycobacterial therapy 2
“M. franklinii” Although 26 clinical isolates were obtained, medical histories were provided for only 6 7
patients; 2 patients had sinusitis, and 4 patients had lower respiratory tract symptoms; all
patients with respiratory tract symptoms had underlying pulmonary disease
M. iranicum Isolated 3 times from the hand wound of an 18-yr-old male with a history of long-term steroid 10
treatment due to renal transplantation; treated with amikacin and clinically improved
An organism grew from culture of a BAL specimen from a 60-yr-old female with pneumonia; 10
patient responded to amikacin and ciprofloxacin
Peritoneal dialysis-related peritonitis in a 68-yr-old male with diabetic nephropathy who 13
responded to appropriate antimycobacterial therapy
HIV-infected patient admitted initially with mild fever, wt loss, chronic chest pain, and 14
nonproductive cough; no AFBa smear was done; patient’s fever and chest pain remained
unchanged; after bronchoscopy, 2 of 3 BAL specimens were AFB smear positive, and 3 of 3
were culture positive for a rapidly growing mycobacterium; a standard antituberculosis
regimen was started, but patient did not improve; after 1 mo, a sputum specimen was
negative for AFB, and 1 BAL specimen was positive by microscopy and culture for M.
iranicum; patient improved rapidly on amikacin and ciprofloxacin for 3 mo
M. longobardum Osteomyelitis of the elbow in a 71-yr-old male 14
M. yongonense First description of the species and its association with pulmonary infection, from the sputum 19
of a patient with unspecified lung disease, was in South Korea
74-yr-old woman presented with fatigue, diarrhea, and wt loss; chest x-ray revealed a cavitary 20
lesion; cultures of sputum and stool grew M. yongonense; a BAL specimen was also AFB
smear positive and grew the same organism
aAFB, acid-fast bacilli.

critical for proper diagnosis and management of infections and for outbreak investi-
gation.
This need was illustrated in recent reports of serious infections in patients who had
undergone open cardiac surgery in which a contaminated heater-cooler device was
used during extracorporeal circulation. These infections, occurring in patients in Europe
and the United States, were caused by Mycobacterium chimaera, a nontuberculous
mycobacterium ubiquitous in soil and water (22). This organism is a slow-growing NTM
species included in the M. avium complex (MAC). Initially, strains of this organism were
identified by a commercial probe assay as Mycobacterium intracellulare. In-depth inves-

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tigation of these strains in 2004 revealed that the organisms were in fact distinct from
M. intracellulare and belonged to a previously unidentified species within the MAC,
namely, M. chimaera (23). Without delineation of this new species, this organism might
have been misidentified and recognition of its association with heater-cooler devices in
the operating room possibly delayed. Despite the already large number of species of
this genus, there is little doubt that this number will continue to increase and that some
newly described species will be recognized to cause infection in humans.

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Betty A. Forbes, Ph.D, is a professor of pathology and internal medicine and


director of the clinical microbiology laboratory at Virginia Commonwealth
University (VCU) Medical Center in Richmond, Virginia. She is a diplomate
of the American Board of Medical Microbiology and a fellow of the Ameri-
can Academy of Microbiology. She has been at VCU Medical Center since

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2003. Previously, she served for 20 years as director of clinical microbiology
at Upstate Medical University in Syracuse, New York. Dr. Forbes graduated
from Northwestern University in 1970. She received her Ph.D. in medical
microbiology and immunology from the University of Oklahoma Health
Science Center in Oklahoma City, Oklahoma, and then completed a 2-year
American Board of Medical Microbiology-approved postdoctoral fellow-
ship program at the University of Michigan, St. Joseph Mercy Hospital, in
Ann Arbor, Michigan. Following her formal fellowship training, she held a
joint appointment with the Division of Infectious Disease, Department of
Internal Medicine, and the Clinical Microbiology Laboratory in the Depart-
ment of Pathology, University of Michigan as a research associate for 2 years.
Dr. Forbes has a special interest in mycobacteria and has published exten-
sively in diagnostics for clinical microbiology. She was an editor for Bailey
and Scott’s Diagnostic Microbiology and an editor in chief for Clinical Micro-
biology Reviews, and she has served as an editor for the Journal of Clinical
Microbiology since 2009.

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