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Hu et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016 17(3):188-199

Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology)

ISSN 1673-1581 (Print); ISSN 1862-1783 (Online)
www.zju.edu.cn/jzus; www.springerlink.com
E-mail: jzus@zju.edu.cn

Review:

Antibiotic resistance mechanisms of Myroides sp.*

Shao-hua HU1, Shu-xing YUAN2, Hai QU3, Tao JIANG1,
Ya-jun ZHOU1, Ming-xi WANG1,4, De-song MING5
(1Yun Leung Laboratory for Molecular Diagnostics, School of Biomedical Sciences and Institute of Molecular Medicine, Huaqiao University /
Engineering Research Center of Molecular Medicine, Ministry of Education, Xiamen 361021, China)
(2Department of Neurosurgery, Linyi Peoples Hospital, Linyi 276000, China)
(3Linyi Health School of Shandong Province, Linyi 276000, China)
4

( Institute of Nanomedicine, Department of Medical Laboratory, Weifang Medical College, Weifang 261053, China)
(5Department of Clinical Laboratory, Quanzhou First Hospital Affiliated to Fujian Medical University, Quanzhou 362000, China)

E-mail: mxwang@hqu.edu.cn; mds6430@126.com

Received Mar. 19, 2015; Revision accepted Nov. 30, 2015; Crosschecked Feb. 15, 2016

Abstract: Bacteria of the genus Myroides (Myroides spp.) are rare opportunistic pathogens. Myroides sp. infections
have been reported mainly in China. Myroides sp. is highly resistant to most available antibiotics, but the resistance
mechanisms are not fully elucidated. Current strain identification methods based on biochemical traits are unable to
identify strains accurately at the species level. While 16S ribosomal RNA (rRNA) gene sequencing can accurately
achieve this, it fails to give information on the status and mechanisms of antibiotic resistance, because the 16S rRNA
sequence contains no information on resistance genes, resistance islands or enzymes. We hypothesized that obtaining the whole genome sequence of Myroides sp., using next generation sequencing methods, would help to clarify
the mechanisms of pathogenesis and antibiotic resistance, and guide antibiotic selection to treat Myroides sp. infections. As Myroides sp. can survive in hospitals and the environment, there is a risk of nosocomial infections and
pandemics. For better management of Myroides sp. infections, it is imperative to apply next generation sequencing
technologies to clarify the antibiotic resistance mechanisms in these bacteria.
Key words: Myroides sp., Antibiotic resistance, Identification methods, 16S ribosomal RNA gene sequencing, Next
generation sequencing
http://dx.doi.org/10.1631/jzus.B1500068
CLC number: R378

1 Introduction

Corresponding authors
The two authors contributed equally to this work
*
Project supported by the Huaqiao University Graduate Student Scientific Research Innovation Ability Cultivation Plan Projects, the
Major Program of Department of Science and Technology of Fujian
Province (No. 2012Y4009), the Science and Technology Planning
Project of Xiamen (No. 3502Z20123036), the Xiamen Southern
Oceanographic Center (No. 14GYY008NF08), the Construction Project for Yun Leung Laboratory for Molecular Diagnostics (No.
14X30127), the Technology Planning Projects of Quanzhou Social
Development Fields (No. 2014Z24), and the Major Support Research
Project of National Key Colleges Construction of Quanzhou Medical
College (No. 2013A13), China
ORCID: Ming-xi WANG, http://orcid.org/0000-0002-8093-0384
Zhejiang University and Springer-Verlag Berlin Heidelberg 2016

The genus Myroides (Myroides spp.) comprises

yellow-pigmented, non-motile, Gram-negative, rodlike bacteria (Holmes et al., 1977; Cho et al., 2011)
that release a fruity odor during growth (Holmes et al.,
1977). The first strain, Stutzer, of the genus Myroides
was isolated from the stools of patients with intestinal
infections (Holmes et al., 1977) and was assigned the
species name Flavobacterium odoratum (Stutzer and
Kwaschnina, 1929). For easier clinical recognition,
the bacteriological features, pigmentation, biochemical characteristics, and antimicrobial profiles of
10 isolates were examined (Holmes et al., 1977).
Myroides spp. were found to be non-fermentative

Hu et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016 17(3):188-199

organisms resistant to many antibiotics (Holmes et al.,

1977). In 1996, after extensive polyphasic taxonomic
analysis of 19 strains of F. odoratum, the genus Myroides was established and included two species, M.
odoratus and M. odoratimimus (Vancanneyt et al.,
1996). Later, more strains were isolated from forest
soil (strain TH-19(T), named M. xuanwuensis sp. nov.
(Zhang et al., 2014)), seawater (strain JS-08(T),
named M. marinus sp. nov. (Cho et al., 2011), strain
SM1(T), named M. pelagicus sp. nov. (Yoon et al.,
2006)), deep-sea sediment (strain D25T (Zhang et al.,
2008)), human saliva (strain MY15T, named M.
phaeus sp. nov. (Yan et al., 2012)), as well as strains
from urine, sputum, surgical exudate (Andreoni,
1986), and patients matter (Table 1). Thus, Myroides
spp. are widely distributed in nature (Mammeri et al.,
2002; Ktari et al., 2012; Suganthi et al., 2013;
Ravindran et al., 2015).
Myroides sp. is a rare opportunistic pathogen
(Schrttner et al., 2014). Nevertheless, management
of Myroides sp. infection is troublesome due to its
high resistance to most antibiotics (as summarized in
Table 1). For accurate strain identification of Myroides sp., current diagnostic methods, such as
the Vitek Jr. system (Vitek Systems, bioMerieux)
(Spanik et al., 1998), are based on bacteriological and
biochemical characteristics, and can determine Myroides sp. at the species level in most cases. However,
they and 16S ribosomal RNA gene sequencing (16S
rRNA sequencing), a standardized bacterial strain
identification method (Yoon et al., 2006; Zhang X.Y.
et al., 2008; Zhang Z.D. et al., 2014) still not widely
applied in Chinese hospitals, fail to provide any information on the status and mechanisms of antibiotic
resistance in Myroides sp. Whole genome sequencing
technologies could address these questions, and
should be applied to Myroides sp. promptly.

2 Antibiotic resistance status of clinical

Myroides sp. infections
Myroides sp. infections are rare. By searching
the PubMed database of English literature using
Myroides or Flavobacterium odoratum as key
words, only a few reports could be found. In immunocompetent people, primary infections by Myroides
sp. have been rarely reported, such as a case of M.

189

odoratimimus cellulitis resulting from a pig bite in an

immunocompetent child (Maraki et al., 2012).
However, secondary infections can frequently arise
when human immunity is impaired, such as post
catheterization (Holmes et al., 1977; Spanik et al.,
1998), in patients with cancer (Holmes et al., 1977;
Spanik et al., 1998; Song, 2005) or diabetes mellitus
(Yang and Wang, 2001), and in neonates (Wang and
Su, 1992; Zhang and Zhang, 1996; Zhao, 2000).
Myroides sp. can cause soft tissue infection (Benedetti et al., 2011), cellulitis (Bachmeyer et al., 2007),
necrotizing fasciitis (Crum-Cianflone et al., 2014),
ventriculitis (Macfarlane et al., 1985), and urinary
tract infections (Yaci et al., 2000). M. odoratimimus
even caused an outbreak of urinary tract infection in a
hospital (Ktari et al., 2012).
By using the same key words to search the China
National Knowledge Infrastructure (CNKI) database,
we found that most reports of Myroides or F. odoratum infections contained a single case (Table 1). Two
papers reported 23 (Table 2) and 11 strains (Table 3),
respectively.
From Tables 1, 2, and 3, we conclude that Myroides spp. are resistant to broad antibiotics, and that
their extensive antibiotic resistance has resulted in
treatment failure and fatalities. We observed a case in
July 2009 in which a patient presented with a post-injury
urinary tract infection caused by M. odoratimimus
strain PR63039 (Table 1, our case). Using antibiotic
sensitivity testing (AST), the strain was found to be
resistant to ampicillin, amoxicillin, clavulanate, amikacin, aztreonam, chloramphenicol, cephalosporin,
imipenem, gentamycin, levofloxacin, meropenem,
shubatan, sulfamethoxazole, tetracycline, ciprofloxacin,
and tazobactam. Even though many antibiotics, such
as cefazolin oxime, amikacin, tetracycline, moxifloxacin, ciprofloxacin, and nitrofurantoin, were administered to the patient for 47 d, the infection was not cured.
The reports analyzed in Table 1 reveal that the
antibiotic resistance of Myroides sp. varies among
strains isolated from different sources. For example, a
strain from a patient suffering from a hydatid cyst of
the liver was sensitive to norfloxacin (An, 1992), but
another strain isolated from pulmonary infection patient was reported to be resistant to norfloxacin (Liu
and He, 2001). Two strains isolated from patients with
cellulitis and a leg amputation, respectively (Hu et al.,
2013; Crum-Cianflone et al., 2014) were resistant to

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ciprofloxacin, while another two isolated from trauma

and septicemia patients, respectively, were sensitive to
ciprofloxacin (Geng et al., 2000; Sun and Zhang, 2006).
Why is there so much variation in the antibiotic
resistance profiles of Myroides sp. strains isolated

from different sources? In our opinion, the subtypes

and genotypes of Myroides sp. might have a great
influence on their sensitivity to certain antibiotics.
Therefore, it is imperative to obtain accurate information on strain subtype and genotype.

Table 1 Summary of reported infections by Myroides sp.

Underlying
Age
Patient
diseases or
Site of isolation
Antibiotic resistance status
(year)/
No.
reasons
gender
1
87/M Trauma,
Wound
Resistant to all antibiotics except
old age
ciprofloxacin. Sensitive to
trimethoprim-sulfamethoxazole
2
34/F Hydatid cyst Drainage
Resistant to neomycin, streptomycin,
of liver
gentamicin, ampicillin, tobramycin.
Sensitive to norfloxacin

ND

ND

Shi and
Zhou,
1993

ND

ND

Guo and
Liu,
2011

71/M Chronic
bronchitis,
old age

Amikacin
Favorable Wu, 1998
Blood, central
venous catheter,
urine
Cured Hu et al.,
28/F Injury and
Wound
Resistant to gentamicin, sulfamethoxazole, Debridement, skin
2013
transplantation, iv
surgery
ciprofloxacin, cefoperazone-sulbactam,
cefperazonetetracycline, tobramycin, cefoperazone,
cefepime, imipenem, piperacillin-tazobactam, sulbactam and
oral minocycline
cefoselis, amikacin, piperacillin,
for 3 d, then oral
levofloxacin, netilmicin, ceftazidime,
cefotaxime, aztreonam, ampicillin-sulbactam. minocycline for
another 3 d
Sensitive to minocycline. Moderately
sensitive to meropenem
Oral minocycline
Cured Huang
Blood, wound
Resistant to piperacillin, ceftazidime,
76/M Chronic
for 9 d
et al.,
ceftriaxone, cefepime, aztreonam,
obstructive
2014
imipenem, meropenem, amikacin,
pulmonary
gentamicin, ciprofloxacin, levofloxacin,
disease and
tetracycline, trimethoprim-sulfamethoxazole,
heart failure,
ampicillin-sulbactam, cefoperazoneold age
sulbactam, piperacillin-tazobactam
Cured Huang
Piperacillin and
4/M None
Blood
Resistant to ampicillin, ampicillinand Lin,
tobramycin for
sulbactam, piperacillin, piperacillin
2003
14 d
tazobactam, aztreonam, cefazolin,
cefoxitin, ceftazidime, cefotaxime, azole
cefepime, ceftazidime, ceftriaxone,
cefepime
Drainage
Sensitive to cefoperazone and amikacin
Incision and drainage, Cured Yang and
58/ND Diabetes
Wang,
cefoperazone and
mellitus
2001
amikacin for
complicated
several days
by heel
(more than 3 d)
bursitis
Cured Song
Abscess incision
28/F None
Pus
Resistant to kanamycin, penicillin,
et al.,
drainage and
erythromycin. Sensitive to ceftriaxone,
1995
norfloxacin and
norfloxacin, trimethoprim-sulfamethoxazole
trimethoprimsulfamethoxazole

10

Sputum

Resistant to cefazolin, penicillin,

chloramphenicol. Sensitive to ampicillin,
polymyxin, kanamycin, erythromycin,
neomycin
Resistant to meropenem, imipenem,
ampicillin, cefradine, tobramycin,
cephalothin, amoxicillin-clavulanic acid,
ampicillin-shubatan, ceftriaxone,
gentamicin, cefoxitin, ceftazidime,
piperacillin. Sensitive to cefepime,
levofloxacin
Sensitive to amikcin, norfloxacin

Norfloxacin

Favorable Sun and

Zhang,
2006
Favorable An, 1992

2/M

Burn

CSF

iv ciprofloxad

30/F

Young age

Treatment strategy Outcome Reference

To be continued

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Table 1
Underlying
Age
Patient
diseases or
Site of isolation
Antibiotic resistance status
(year)/
No.
reasons
gender
11
24 d/M Neonate
Blood
Resistant to penicillin, chloramphenicol,
carbenicillin, streptomycin, cefazolin.
Sensitive to amikacin, erythromycin,
ampicillin, benzylpencilline
12
11 d/M Preterm birth Blood, CSF
Resistant to ampicillin, cefazolin,
gentamicin, cefoperazone, cefotaxime,
cefatrizine, ceftazidime. Sensitive to
amikacin, piperacillin, ampicillin,
sulbactam-cefoperazone
Resistant to tobramycin, gentamicin,
13
69/F Lung cancer Pleural effusion
ampicillin, erythromycin, clindamycin,
and surgery, and sputum
tetracycline. Sensitive to amikacin,
old age
tobramycin, ceftriaxone
14 10 months/ Child
Blood
Sensitive gentamicin, tobramycin,
F
cephalexin, sulbactam-cefoperazone,
ceftriaxone
Resistant to tobramycin. Sensitive to
15
60/M Common bile Blood, bile,
piperacillin, cefoperazone, amikacin,
duct stones peritoneal
gentamicin, ceftriaxone, cefotaxime
effusion
16

44/F

None

17

67/M

Old age

18

45/M

None

19

N/A

ND

20

ND

21

ND

22

ND/F

23

61/F

Blood, bone
Sensitive to norfloxacin, ciprofloxacin,
marrow
cefazolin, amikacin, ceftazidime
Sputum (this strain Resistant to ampicillin, piperacillin
cefazolin, cefuroxime, cefotaxime,
was isolated
ceftazidime, cefotaxime, aztreonam,
with Serratia
gentamicin, norfloxacin,
marcescens,
trimethoprim-sulfamethoxazole
Acinetobacter
lwoffi)
Urine
Resistant to ampicillin, amikacin,
azithromycin

Treatment strategy Outcome Reference

Ampicillin, and
oxacillin for 19 d

Cured

Wang and
Su,
1992

Antimicrobial
treatment for 5 d
(the antibiotic was
not described)

Failed

Zhang and
Zhang,
1996

Antimicrobial
treatment, but not
described in detail

Died

Song,
2005

Cefoperazone,
tobramycin for
10 d
Amikacin and
cefoperazone

Cured

Zhao,
2000

Cured

Meng
et al.,
1999

ND

ND

Geng et al.,
2000
Liu and
He,
2001

Antimicrobial
treatment, but not
described in detail

Cured

Application of
cefoperazone,
cefotaxime,
nitrofurantoin,
and tobramycin
for 3 weeks
N/A

Cured

Wuer
et al.,
2000

N/A

Li and
Zhao,
1995

ND

Li et al.,
2010

Died

Jin and
Xiao,
1995

Blood, sputum,
All 12 isolates were resistant to
bile, cerebrospinal erythromycin, penicillin, streptomycin,
ampicillin, oxacillin, piperacillin,
fluid, urine, all
carbenicillin
these three
isolates were
from patients (no
further details
were available)
Chronic
Urine
Two isolates were resistant to meropenem. One isolate was
sensitive to
nephritis
All three isolates were resistant to
Diabetes
meropenem
ampicillin-sulbactam, piperacillinmellitus
tazobactam, cefuroxime, cefotetan,
Cervical
ceftriaxone, aztreonam, gentamicin,
cancer
ciprofloxacin, levofloxacin, ampicillin,
piperacillin, cefazolin, cefuroxime axetil,
ceftazidime, cefepime, imipenem,
amikacin, tobramycin, levofloxacin,
trimethoprim-sulfamethoxazole
Sputum
N/A
Ceftazidine,
Coma,
chloramphenicol,
cerebral
penicillin G,
hemorrhage
gentamicin by
atomization
inhalation,
ketoconazole by
nasal feeding

To be continued

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Table 1
Age
Underlying
Patient
(year)/
diseases or
Site of isolation
Antibiotic resistance status
No.
gender
reasons
24
49/M Chronic alcohol Blood
Intermediately sensitive to imipenem
misuse

25

55/F Liver cirrhosis Blood, wound

bilateral lower
extremity
cellulitis and
open wounds

26

13/M Soft tissue

infection

27
28
29
30
31
32
33
34
35
36
37
38
39
40
41

Pus

48/F Cystitis
Urine
(contaminated)
34/M Infected cut
Wound
finger
59/F ND
Urine
ND/ND Urinary
Urine
retention
ND/ND Further details Urine
are not
available
ND/ND Varicose ulcer Wound
76/F Leg ulcer
Ulcer
67/F Breast lump
Urine
48/M Chronic renal Urine
insufficiency
66/M Urinary tract
Urine
infection
44/M Bladder
Urine
44/M
colonization Urine
47/M
Urine
77/M Urinary tract
Urine
infection
65/M
Urine

42

80/M

Urine

43

59/M Urinary tract

infection

Urine

Treatment strategy

Outcome Reference

Cured Bachmeyer
Treatment with
et al.,
amoxicillin2007
clavulanic acid was
changed to
ciprofloxacin,
imipenem-cilastatin
used for 10 d, then
oral ciprofloxacin
for 21 d
Resistant to amikacin, gentamicin,
iv vancomycin,
Died Crumtobramycin, aztreonam, ceftriaxone,
piperacillinCianflone
ciprofloxacin, tetracycline,
tazobactam, and
et al.,
trimethoprim-sulfamethoxazole,
levofloxacin for
2014
vancomycin. Intermediately sensitive
18 h, then iv
to piperacillin-tazobactam, cefepime,
imipenem-cilastatin,
imipenem, and cilastatin
daptomycin,
clindamycin, then
imipenem-cilastatin
and doxycycline
Resistant to piperacillin-tazobactam,
Drainage of osteolytic Cured Maraki
aztreonamaminoglycosides.
lesions combined
et al.,
Intermediately susceptible to
with iv ciprofloxacin
2012
imipenem. Sensitive to all quinolones
for 10 d and
tested, cotrimoxazole,
continued with oral
chloramphenicol, and
ciprofloxacin for an
amoxicillin-clavulanic acid
additional 10 d
Fully resistant to streptomycin,
N/A
N/A Holmes
gentamicin, kanamycin, ampicillin,
et al.,
carbenicillin, tetracycline,
1977
polymyxin B.
Fully resistant or moderately resistant to
sulfamethoxazole, trimethoprimsulfamethoxazole, cephaloridine,
erythromycin, chloramphenicol.
Moderately sensitive to nalidixic acid

Resistant to all -lactam and non-lactam antibiotics tested, including

imipenem, vancomycin,
ciprofloxacin, chloramphenicol,
tigecycline, rifampicin

Resistant to amikacin, gentamicin,

imipenem, meropenem, cefazolin,
ceftazidime, cefotaxime, cefepime,
aztreonam, ampicilllin, piperacillin,
amoxicillin-clavulanate, ampicillinsulbactam, piperacillin-tazobactam,
colistin, trimethoprimsulfamethoxazole, chloramphenicol,
ciprofloxacin, levofloxacin,
moxifloxacin, tetracycline

Imipenem, colistin

Failure Ktari et al.,

2012
Favorable
Favorable
Favorable
Cured

No treatment
No treatment
No treatment
Ifampicin
ciprofloxacin
Ifampicin
Cured
ciprofloxacin
Ifampicin
Cured
ciprofloxacin
Levofloxacin was used Failure Our case
only temporarily
and orally

M: male; F: female; N/A: not applicable; ND: not described; CSF: cerebrospinal fluid; iv: intravenous injection

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Table 2 Antimicrobial susceptibility testing of 23 strains of Myroides sp. using the K-B method
Site of isolation (total samples of positive isolation)
Sputum (8);
Urine (6);
Blood (4);
CSF (3);
Bile (2)

Antibiotic
Amikacin

R
5

I
10

S
8

Cefazolin

11

Cefoperazone

Sulfamethoxazole

10

Sulfadiazine

11

Ceftazidime

10

Erythrocin

10

10

Azithromycin

10

Translated from Lan and Bao (2009) with permission of the authors. K-B method: Kirby-Bauer disk diffusion method; CSF: cerebrospinal fluid; R: resistant; I: immediately sensitive; S: sensitive

Table 3 Antimicrobial susceptibility testing of 11 strains of Myroides sp. isolated from urine using Oxoid culture medium
Patient information
276 years (average 53 years), 9 males, 2 females
All patients suffered from urinary retention or
urinary tract stones, but none of them had
symptoms of urinary tract infection or other
discomfort
In nine urinarily catheterized patients, the urinary
culture when the catheter was in situ was Myroides
sp. positive, but the urinary testing showed no
WBC in these urinary samples, and pus cells were
found in only three of them
The urinary culture of Myroides sp. became negative
after removal of urinary catheter in these nine
urinarily catheterized patients even though they
were not treated

Ampicillin

Antibiotic

R
11

I
0

S
0

Piperacillin

11

Cefuroxime

11

Cefoperazone-sulbactam

11

Ceftazidine

10

Cefepime

10

Aztreonam

11

Imipenem

11

Meropenem

11

Levofloxacin

Ciprofloxacin

Trimethoprim-sulphamethoxazole

11

Amikacin

11

Translated from Chen et al. (2009) with permission of Chin. J. Pract. Med. Tech. R: resistant; I: immediately sensitive; S: sensitive; WBC:
white blood cell

3 Preliminary opinions on the antibiotic resistance mechanisms of Myroides sp.

In China, there have been no reports on the antibiotic resistance mechanisms of Myroides sp. Although several foreign researchers have investigated
this topic, very little information is available. Hummel et al. (2007) showed that the -lactamase gene
was responsible for the variable patterns of resistance
to -lactam antibiotics and the decreased susceptibility to carbapenems of different Myroides sp. strains.
In a study investigating a number of clinical cases

involving systemic infections, Mammeri et al. (2002)

claimed that resistance to -lactams was due to the
production of the chromosome-encoded -lactamases
TUS-1 and MUS-1 in M. odoratus and M. odoratimimus. The -lactamases produced by Gram-negative
and Gram-positive bacteria play a vital role in resistance against -lactam antibiotics. However, their
study showed that the -lactamases TUS-1 and
MUS-1 could only partly explain the intrinsic resistance of Flavobacteriaceae species to -lactams.
Also, a common observation was that these Escherichia coli expressed metalloenzymes were much

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less resistant to -lactam than those of primitive

origin (Mammeri et al., 2002). Even Flavobacteriaceae and Myroides sp. belong to the same family, the
mechanism of resistance conferred by TUS-1 and
MUS-1 in Flavobacteriaceae species cannot be assumed to operate in Myroides sp. Then, why does
Flavobacteriaceae serve as a source for a variety of
metalloenzymes? As observed for other environmental species, this might be due to the combined
biosynthesis of carbapenem derivatives and hydrolyzing -lactamases (Mammeri et al., 2002).
Suganthi et al. (2013) investigated whether the
antibiotic sensitivity of plasmid-containing M. odoratimimus SKS05-GRD was correlated with the
plasmid or was chromosomally-mediated. They revealed that resistance to kanamycin, amikacin, and
gentamicin was plasmid-mediated, and that resistance
to ampicillin, cefadroxil, cefoperazone, ceftazidine,
ceftriaxone, and netillin was chromosomally-mediated.
The Klebsiella pneumoniae carbapenemase (KPC)
family is closely related to resistance to carbapenem
in a variety of pathogens and the KPC gene is located
in a plasmid. However, Myroides sp. WX2856, obtained from an abdominal abscess (Kuai et al., 2011),
harbored a KPC-2 carbapenemase, but the KPC-2
gene might not be located on a plasmid as in K.
pneumoniae. Do these results suggest the possibility
of interspecies transmission of the KPC-2 gene? This
aspect needs further investigation.
On the other hand, there are several known features of antibiotic resistance mechanisms in bacteria
from the same family of Myroides, such as in F. indologenes, now named Chryserobacterium indologenes (Tian and Wang, 2010). First, resistance
transfer factors (R-factors) in the cytoplasm determine the bacterias resistance to antibiotics. R-factor
plasmids can carry and transfer a variety of resistance
genes among bacteria. In addition, the thick outer
membrane and its low permeability, resulting from
multidirectional mutations, and the active discharge
system of the bacterial cell membrane of C. indologenes confer inherent multi-drug resistance. The
bacteria also produce a -lactamase with a broad
spectrum of -lactam hydrolytic activity (Tian and
Wang, 2010).
Thus, it is apparent that the antibiotic resistance
mechanisms of Myroides sp. are unclear and deserve
further investigation.

4 Present diagnostic methods do not clarify

the antibiotic resistance mechanisms of
Myroides sp.
In clinical diagnostic laboratories, traditional
bacterial identification methods primarily rely on
testing biological traits and biochemical characteristics, and include microscopic inspection and metabolic testing of isolated and cultured bacteria. These
methods have shown that Myroides spp. do not have
flagella, release a fruity fragrance, are yellow, oxidasepositive, urea- and indole-negative, and are unable to
oxidize sugar (Li and Zhao, 1995; Chen et al., 2009).
However, the bacterial strain can be preliminarily
identified only as Myroides sp., as further strain type
designations cannot be determined using these traditional methods. Nearly all cases of Myroides sp. infections reported in China have used these traditional
identification approaches, and did not describe any
Myroides sp. subtypes. Using these traditional identification methods, the M. odoratimimus strain
PR63039 isolated in our case was first identified as
Pseudomonas putida, then as M. odoratimimus, and
as the Acinetobacter calcoaceticus-baumannii complex, at different time points throughout the 47 d of
the patients hospitalization. It was finally confirmed
as M. odoratimimus by 16S rRNA sequencing. This
case also indicates that these traditional identification
methods may not correctly diagnose the strain type.
Recently, other microorganism strain identification technologies have been developed, including
VITEK 2 (bioMerieux VITEK-2, France), matrixassisted laser desorption/ionization time-of-flight mass
spectrometry (MALDI-TOF MS), 16S rDNA sequencing, and another more frequently used nomenclature, 16S rRNA sequencing (Table 4). VITEK 2, a
routine laboratory method, can help to discriminate
among genera but not among species. MALDI-TOF
MS and 16S rDNA sequencing/16S rRNA sequencing can be used to identify species and are more frequently used for research purposes (Lee et al., 2014;
Schrttner et al., 2014). According to Schrttner et al.
(2014), the genus Myroides was reliably identified in
tests of 22 isolates using VITEK 2. 16S rDNA sequencing further revealed that they shared 97%
homology, enough for a reliable identification at the
species level. Yoon et al. (2006) applied 16S rRNA
sequencing successfully to clarify the phylogenetic

Hu et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016 17(3):188-199

position of Myroides sp. strain SM1T, isolated from

seawater in Thailand.
Table 4 Comparison of the present approaches for
strain identification of Myroides sp.*
Method
VITEK2

MALDI-TOF MS

Trait
Only suitable to identify bacteria at
the genus level, not at the species
level
Able to distinguish between M.
odoratus and M. odoratimimus
Able to distinguish microorganisms
at the species level

16S rDNA
sequencing/16S
rRNA sequencing
Whole genome
Able to identify the microorganism
sequencing
and provide the bioinformatics of
microorganism
*

Yoon et al., 2006; Lee et al., 2014; Schrttner et al., 2014

5 Whole genome sequencing is a feasible

way to investigate the antibiotic resistance
mechanisms of Myroides sp.
In the past decade, many next generation sequencing platforms have been developed, such as 454
invented in 2004 (Margulies et al., 2005), Illumina
Solexa in 2006 (Bentley, 2006), SOLiD in 2007
(Chi, 2008), Ion Torrent in 2011 (Rothberg et al.,
2011), and PacBio in 2012 (Koren et al., 2012). This
has led to a rapid increase in the sequencing of whole
genomes of microorganisms, including eukarya,
bacteria, archaea, and viruses. These sequences have
been deposited in the National Center for Biotechnology Information (NCBI) RefSeq genome collection database (http://www.ncbi.nlm.nih.gov/genome)
(Tatusova et al., 2015). In 2014, over 10 000 microbial genomes were released (Tatusova et al., 2015).
Along with the next generation platforms, wholegenome analysis of multi-drug resistance mechanisms
has emerged.
For example, A. baumannii is a common cause
of fatal nosocomial infections because of its extensive
antibiotic resistance. Genomic sequencing revealed
comprehensive drug-resistance mechanisms, such as
a 41.6-kb closely related antibiotic resistance island
in the chromosome (Huang et al., 2012), the horizontally transmittable carbapenem resistance gene
(blaOXA-23) containing a plasmid (in isolate MDR-TJ,

195

with 454 Titanium) among different A. baumannii

strains (Huang et al., 2012; Lee et al., 2013), a list of
antimicrobial resistance-associated genes (with 454
and SOLiD) (Rolain et al., 2013), a diversified resistance gene list (with Illumina Hiseq2000) (Tan
et al., 2013), and longitudinally evolved antibiotic
resistance gene mutations and mutational pathways
under pressure from the antibiotic colistin (with 454
Titanium) (Snitkin et al., 2013). Since its invention by
Rothberg et al. (2011), Ion Torrent sequencing technology has been successfully applied to complete
genomic sequencing, such as in Clostridium sp. BL8
(with Ion Torrent PGM) (Marathe et al., 2014), and
clear characterization of drug-resistant genes, such as
in Mycobacterium tuberculosis (Daum et al., 2014).
Results can be obtained within five days, comparable
to the turnaround time required by current drug sensitivity testing (DST) (Daum et al., 2014). PacBio
single-molecule real-time technology has frequently
been used to perform whole-genome sequencing of
many microorganisms, such as Neisseria gonorrhea
(with the PacBio RSII platform), a Gram-negative
proteobacterium responsible for the sexually transmitted infection gonorrhea (Abrams et al., 2015).
Yet, little genomic information about Myroides
sp. is available. A brief description of the genomes of
M. odoratus DSM 2801 and CIP 103059 was found in
genome database of NCBI (Table 5), but this was not
suitable for studying its drug-resistance mechanisms.
Recently, the genome sequencing of the urethral
catheter isolate Myroides sp. A21 was completed
(Burghartz et al., 2015). The sequence contained
3650 protein-coding sequences (CDSs), 136 RNAcoding genes, and eight copies of the rRNA gene
cluster, of which three were resolved as a direct repeat
of two rRNA gene clusters. The presence of 106
transfer RNAs (tRNAs) and six noncoding RNAs
(ncRNAs) was also predicted. By comparing the genome sequence of Myroides sp. A21 with those of M.
odoratimimus CCUG 10230 and M. odoratus DSM
2801, 293 unique CDSs were found in the A21 genome (Burghartz et al., 2015). In addition, five genomic islands were predicted by Island Viewer analysis (Burghartz et al., 2015). However, as the antibiotic treatment history was not described and the antibiotic resistance status of this strain was not given,
the antibiotic resistance mechanisms could not be
analyzed from the data.

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Hu et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016 17(3):188-199

Table 5 Reported RefSeq genome of Myroides odoratus CIP 103059 and DSM 2801
Strain
CIP 103059
DSM 2801

Name

RefSeq

INSDC

Master NZ_AGZJ000000 AGZJ000000

WGS
00.1
00.1
NZ_CM001437.1 CM001437.1

Size
(Mb)
4.23
4.3

Total
Total
number of number of rRNA
proteins
genes
3773
3631
10
3838

3695

tRNA
67
74

GC
Other
content Pseudogenes
genes
(%)
1
35.8
64
1

35.8

59

Cited from GenBank assembly accession: GCA_000243275.1 and GCA_000297875.1. INSDC: International Nucleotide Sequence Database
Collaboration

To study these aspects in our M. odoratimimus

strain PR63039, we extracted its genomic DNA.
Agarose gel electrophoresis results from several experiments revealed that it might harbor at least six
different types of plasmids which could be related to
antibiotic resistance (Fig. 1). However, the exact
number of plasmid type needs further confirmation.
Many bacterial drug-resistance genes are plasmid- or
chromosome-mediated, but we did not know which
mechanism was operating in Myroides sp. The genome of strain PR63039 was sequenced using an Ion
Torrent Personal Genome Machine. We generated
610 contigs and 4221 open reading frames. The total
sequence numbers with Gene Ontology (GO) and
Clusters of Orthologous Groups (COG) of protein
were 2741 and 1026, respectively. However, we
could not completely assemble the genome and
plasmids, so the multi-drug resistance mechanisms of
strain PR63039 still could not be clarified. We are
now using PacBio single-molecule real-time technology in the hope of generating a complete genome
sequence of both the chromosome and plasmids, to
elucidate the mechanisms of resistance and pathogenesis of this strain.
All the infection reports from China indicated
that Myroides sp. is a serious source of nosocomial
infection and has the potential to cause a pandemic.
The completion of the Myroides sp. genome sequence
and detailed bioinformatics analysis are imperative
for the understanding of its mechanisms of antibiotic
resistance and pathogenesis.

6 Discussion and outlook

Myroides sp. is an opportunistic and extensively
antibiotic-resistant pathogen. Infections have not
been widely reported, though there have been many
cases in China. As the antibiotic resistance mechanisms of Myroides sp. are still unclear, and in view of
the risk of nosocomial infection and pandemics,

Fig. 1 Agarose gel electrophoresis of genomic DNA of

Myroides odoratimimus strain PR63039
The genomic DNA of PR63039 was separated by gel electrophoresis using 0.75% (7.5 g/ml) agarose. The genomic
DNA was about 23 kb in size. M1: 1 kb DNA marker; M2:
DNA marker-G; A: 0.173 g DNA; B: 0.273 g DNA; C:
0.328 g DNA. The genomic DNA was about 23 kb in size.
Six different types of plasmids (16) were visible

novel technologies, such as whole genome sequencing and further bioinformatic analyses, should be
applied urgently to Myroides sp. An outline of a
strategy for whole genome sequencing and bioinformatic analyses is presented in Fig. 2. These analyses will also be helpful in developing appropriate
management strategies. Moreover, whole genome
sequencing might become a routine diagnosis method
for all microbial infections in the near future.
Compliance with ethics guidelines
Shao-hua HU, Shu-xing YUAN, Hai QU, Tao JIANG,
Ya-jun ZHOU, Ming-xi WANG, and De-song MING declare
that they have no conflict of interest.
This article does not contain any studies with human or
animal subjects performed by any of the authors.

Hu et al. / J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016 17(3):188-199

197

Fig. 2 Procedure of the strategy of whole genome sequencing and bioinformatics analyses
COG: Clusters of Orthologous Group; GO: Gene Ontology; KEGG: kyoto encyclopedia of genes and genome;
ARDB: Antibiotic Resistance Genes Database; VFDB: Virulence Factor Database; CARD: Comprehensive Antibiotic Research Database; ncRNA: noncoding RNA; ORF: open reading frame

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16S rRNA