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. 2018 Jan 18;6(1):10.1128/microbiolspec.arba-0005-2017. doi: 10.1128/microbiolspec.arba-0005-2017

Antimicrobial Resistance in Stenotrophomonas spp

Yang Wang 1, Tao He 2, Zhangqi Shen 3, Congming Wu 4
Editors: Frank Møller Aarestrup5, Stefan Schwarz6, Jianzhong Shen7, Lina Cavaco8
PMCID: PMC11633551  PMID: 29350131

ABSTRACT

Bacteria of the genus Stenotrophomonas are found throughout the environment, in close association with soil, sewage, and plants. Stenotrophomonas maltophilia, the first member of this genus, is the predominant species, observed in soil, water, plants, animals, and humans. It is also an opportunistic pathogen associated with the increased number of infections in both humans and animals in recent years. In this article, we summarize all Stenotrophomonas species (mainly S. maltophilia) isolated from animals and food products of animal origin and further distinguish all isolates based on antimicrobial susceptibility and resistance phenotypes. The various mechanisms of both intrinsic and acquired antimicrobial resistance, which were mainly identified in S. maltophilia isolates of nosocomial infections, have been classified as follows: multidrug efflux pumps; resistance to β-lactams, aminoglycosides, quinolones, trimethoprim-sulfamethoxazole, and phenicols; and alteration of lipopolysaccharide and two-component regulatory systems. The dissemination, coselection, and persistence of resistance determinants among S. maltophilia isolates have also been elaborated.

INTRODUCTION

The genus Stenotrophomonas comprises 16 characterized species (Table 1), and 13 validated species are included in the List of Prokaryotic names with Standing in Nomenclature (1). The first Stenotrophomonas species—Stenotrophomonas maltophilia—was isolated in 1943 from human pleural fluid. It was classified as Bacterium bookeri and subsequently renamed Pseudomonas maltophilia/Xanthomonas maltophilia (1, 2). Another 12 Stenotrophomonas species were first identified residing in soil, sewage, or plants. Of the remaining three species, Stenotrophomonas sp. D-1 and Stenotrophomonas koreensis were first isolated from deer fur and animal compost, respectively, and Stenotrophomonas africana was initially isolated from a sample of cerebrospinal fluid from a human immunodeficiency virus seropositive Rwandan refugee with primary meningoencephalitis (3). S. maltophilia is the most widely distributed bacterium of the Stenotrophomonas spp. in the environment and is isolated from soil, water, plants, animals, and humans. Moreover, the number of nosocomial infections caused by this opportunistic pathogen is increasing (4). Therefore, various studies of Stenotrophomonas in both animals and humans focus on the emergence, infections, treatment, and antimicrobial resistance of S. maltophilia as an opportunistic pathogen (4, 5). The main purpose of this article is to describe the antimicrobial resistance of S. maltophilia isolated from animals.

TABLE 1.

Characterization of Stenotrophomonas species

Species Year of first identification/designation Host when first identified Characterization Countries/continents Ref.
S. maltophilia 1943 Human S. maltophilia, a new bacterial genus for X. maltophilia, is first identified from a specimen of pleural fluid England/Europe 99
S. africana 1997 Human Opportunistic pathogen from cerebrospinal fluid Rwanda/Africa 3
S. nitritireducens 2000 Ammonia-supplied biofilters It reduced nitrite, but not nitrate, without production of nitrogen Germany/Europe 100
S. sp. D-1 2002 Animal (deer fur) A keratin-degrading bacterium isolated from soil containing deer fur; 16S rDNA revealed it has only 90.6% homology with S. nitritireducens Japan/Asia 101
S. acidaminiphila 2002 Upflow anaerobic sludge blanket (UASB) reactor A strictly aerobic, mesophilic bacterium isolated from UASB reactor treating a petrochemical wastewater Burkina Faso/Africa 102
S. rhizophila 2002 Environment (plant) Plant-associated bacterium with antifungal properties Germany/Europe 103
S. dokdonensis 2006 Environment (soil) The levels of 16S rDNA sequence similarity between S. dokdonensis and the type strains of Stenotrophomonas species ranged from 95.5 to 97.5% Korea/Asia 104
S. koreensis 2006 Environment (animal compost) A Gram-negative, rod-shaped, non-spore-forming bacterium was isolated from compost near Daejeon city Korea/Asia 105
S. humi 2007 Environment (soil) The nitrate-reducing bacterium was isolated from soil Belgium/Europe 106
S. terrae 2007 Environment (soil) The nitrate-reducing bacterium was isolated from soil Belgium/Europe 106
S. chelatiphaga 2009 Environment (sewage) An EDTA-utilizing gammaproteobacterial strain was isolated from municipal sewage sludge Russia/Europe 107
S. ginsengisoli 2010 Environment (soil) A Gram-negative, non-spore-forming, rod-shaped bacterium was isolated from soil from a ginseng field Korea/Asia 108
S. daejeonensis 2011 Environment (sewage) Comparative 16S rDNA analysis showed it was related most closely to S. acidaminiphila (97.9% similarity) Korea/Asia 109
S. pavanii 2011 Environment (plant) A Gram-negative, rod-shaped, non-spore-forming, and nitrogen-fixing bacterium was isolated from stems of a Brazilian sugar cane variety Brazil/South America 110
S. tumulicola 2015 Environment (spot and gels) A major contaminant of the stone chamber interior in blackish moldy spots and viscous gels (biofilms) collected from both tumuli Japan/Asia 111
S. sp. DDT-1 2016 Environment (contaminated soil) A novel bacterium capable of utilizing 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane (DDT) as the sole carbon and energy source. China/Asia 112
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The earliest study of S. maltophilia reported its isolation from sources associated with rabbits, raw milk, and frozen fish in 1961 (6). It is the predominant bacterial species in swine and chicken feces (7), as well as in composted swine manure (8). S. maltophilia isolates have been found to coexist with influenza virus in the oral, nasal, and tracheal tissues of pigs and horses (9, 10). S. maltophilia is a predominant bacterial species in raw milk, milk processing plants, and milk products such as cheese (11–13) and is likely a constituent of the normal microflora of the mouth and cloacae of squirrels and captive healthy snakes (14, 15). In aquaculture, Stenotrophomonas spp. are predominant members of bacterial communities found in the internal organs of cultured snow crabs (Chionoecetes) (16) and are commonly isolated from cultured yellowtail (17), shrimp (18), and samples taken from salmon farms (19, 20).

Although Stenotrophomonas spp. are less frequently considered as primary pathogens, S. maltophilia is the major cause of the bacteriospermia in porcine or bovine semen in the United States and United Kingdom (21–23), as well as the infection of Xenopus laevis oocytes (24). It was also found to be associated with an outbreak of lymphadenitis in Omani goats (25) and causes fleece rot in sheep (26). Closely related S. maltophilia strains were isolated from an outbreak of bovine mastitis (27), which may be explained by the higher adhesion of these isolates to bovine mammary gland epithelial cells (28). S. maltophilia was identified as a cause of pyogranulomatous hepatitis in a female buffalo (Bubalus bubalis) in a herd in Serres, Greece (29), as well as the cause of necrosis and friability of the nictitating membrane of the giant panda (Ailuropoda melanoleuca) (30). It is also associated with chronic respiratory disease among horses, dogs, and cats (31, 32), as well as septicemia in pigs and crocodiles (33, 34). Moreover, the DNA of S. maltophilia is identified most frequently in the knee joints of dogs with inflammatory arthritis (35).

ANTIMICROBIAL SUSCEPTIBILITY

The susceptibility testing methods for S. maltophilia include disk diffusion, agar/broth dilution, commercially available microdilution strips, and microtiter panels (Table 2). Although the Clinical Laboratory Standards Institute (CLSI) has not defined breakpoints for S. maltophilia isolated from animals, the breakpoints for human isolates of S. maltophilia for sulfamethoxazole/trimethoprim (SXT), minocycline, levofloxacin, ticarcillin-clavulanic acid, ceftazidime, and chloramphenicol have been commonly adopted (36). The breakpoints for Enterobacteriaceae and Pseudomonas spp. are also frequently employed to interpret the susceptibility data for S. maltophilia (29, 32). Other breakpoints, such as those specified by the National Reference Laboratory for Antibiotics (National Institute of Public Health, Prague, Czech Republic) and the Antibiogram Committee of the French Microbiology Society, have also been used (13, 15).

TABLE 2.

Antimicrobial resistance of S. maltophilia isolated from animals and animal products

Origin Year of identification Country Strain no. Standards and methods of susceptibility testinga Antimicrobial agents used for susceptibility testing (resistance rates, %)b Ref.
β-Lactams (penicillins, cephalosporins, carbapenems) Macrolides Phenicols Aminoglycosides Tetracyclines Fluoroquinolones Polymyxins Lincosamides/glycopeptides Sulfonamides
Swine semen 2000 USA 6 NCCLS M31-A, 1999; disk diffusion AMP (100) ERY (100) and TIL (100) GEN and SPT (100) OTC (100) CL (0) Triple sulfa (100) 21
Omani goats 2003 Oman 15 NCCLS M2-A4, 1992; disk diffusion PEN, AMP, AMC, and TIC (100) CAZ, CTX, and CEP (100) ERY (0) CHL (0) KAN, GEN, and AMK (0) TET (0) ENO (0) SXT (0) 25
Salmon farm 2003 Chile 1 NCCLS M7-A5, 1998; agar dilution OTC (R), DOX (R), MIN (S) 19
Yellowtail (Seriola quinqueradiata) 2005 Japan 6 Sensi-Disks (Showa, Tokyo, Japan); disk diffusion AMP (100)CTX and CAZ (100) 17
13-lined ground squirrel 2007 USA 1 Clinical Microbiology Procedures Handbook; broth microdilution AMP and AMX (R) CHL (R) GEN and SPT (R) TET (R) 14, 113
Captive snakesc 2007 Czech Republic 47 NCCLS M2-A8, 2003; breakpoints from National Reference Laboratory for Antibiotics (National Institute of Public Health, Prague, Czech Republic); broth microdilution AMP (87.2), ATM (89.4), CAZ (68.1), CFP (63.8), CFZ (95.7), CPS (51.1), CTX (85.1), CXM (95.7), FEP (80.9), FOX (95.7), MEM (74.5), PIP (48.3), SAM (68.1), TZP (36.2) CHL (61.7) AMK (31.9), GEN (25.5), TOB (57.4) TET (89.4) LVX (0), OFX (2.1), CIP (42.6) CL (21.3) SXT (2.1) 15
Horse, cat, dog, and python 2009 Germany 7 Automated susceptibility test strips ATB PSE 5 and ATB VET strips (BioMérieux); microdilution TIC, PIP, IPM, and CAZ (100) CHL (28.6) AMK (42.9), GEN (71.4), TOB (57.1) TET (100) CIP and ENO (0) CL (0) SXT (14.3) 31
Giant panda 2010 USA 1 Unknown AMC, AMP, CAZ, CTX, CEF, and CEP (R) AZI (R) CHL (S) GEN, NEO, and TOB (R) DOX (S) OTC and TET (R) CIP and ENO (S) CL (R) CLI and VAN (R) SXT (I) 30
Captive snakes 2010 Czech Republic 45 CLSI M100-S19, 2009; broth microdilution CAZ (44.4) CHL (28.9) LVX (0) SMX (2.2) 37
Buffalo (Bubalus bubalis) 2010 Greece 1 CLSI M100-S15, 2005; breakpoints of Pseudomonas spp. used; broth microdilution TIC and PIP (R)CAZ and IPM (R) CHL (S) AMK, GEN, and TOB (R) TET (R) CIP and ENO (S) CL (S) SXT (S) (29)
Horse 2010 Denmark 7 CLSI M100-S13, 2003; broth microdilution PEN, AMP, and AMC (100)CF, CPD, and IPM (100) ERY (100) GEN and AMK (100) TET (0) MAR and ENO (0) SXT (0) 32
Oocytes of Xenopus laevis 2011 USA 5 Unknown; disk diffusion AMX, AMC, and TIC (100), CZ, CF, CTX, CPD, CEF, CXM, and CN (100) CRO (80), CAZ and IPM (0) CHL (100) GEN and TOB (100) AMK (0) TET (100) CIP (0)DIF, ENO, OFX, and OBX (100) MAR (80) 24
Milk and Cheese 2012 France 3 Antibiogram Committee of the French Microbiology Society (CA-SFM), 2008/2009; disk diffusion AM, PIP, AMX, AMC, TIM, CTX, and CAZ (100)IPM (66.7) CHL (100) TET (100) 13
Pig 2012 China 7 Unknown; disk diffusion AMP, AMX, and novobiocin (100) CTX and CAZ (100) GEN and STR (100) S3 and TMP (100) 10
Bovine mastitis 2012 Japan 13 CLSI M31-A3 (2008) and M100-S21 (2011); commercially prepared microtiter panel (Opt Panel MP) and disk diffusion MOX (0), CAZ (92.3) CHL (7.7) CIP (7.7)ENO (0) SXT (15.4) 27
Pig 2015 China 1 CLSI VET01-A4 (2013) and M100-S24 (2014); broth microdilution AMP, AMC, CEF, CAZ, and MEM (R) ERY and AZI (R) CHL and FFC (R) GEN, STR, and SPT (R) TET and DOX (R) ENO (R), LVX (I), CIP (R) CL (R) SMX and SXT (R) 33
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a

For more than one strain, the resistance rate was calculated, and the susceptibility results were interpreted as resistant/intermediate/susceptible (R/I/S) for single strains. CLSI breakpoints were only available for S. maltophilia from humans for SXT, MIN, LEV, TIM, CAZ, SXT, and CHL determined using disk diffusion or dilution methods. For other antimicrobials, the breakpoints for Enterobacteriaceae or Pseudomonas spp. were used to interpret the susceptibility results for S. maltophilia.

b

PEN, penicillin G; AMP, ampicillin; AMX, amoxicillin; PIP, piperacillin; TIC, ticarcillin; TIM, ticarcillin/clavulanic acid; AMC, amoxycillin/clavulanic acid; SAM, ampicillin/sulbactam; TZP, piperacillin/tazobactam; CAZ, ceftazidime; CTX, cefotaxime; CEF, ceftiofur; CEP, cephalothin; CFZ, cefazolin; CFP, cefoperazone; CN, cephalexin; CRO, ceftriaxone; CPS, cefoperazone/sulbactam; CF, cephalothin; CXM, cefuroxime; FEP, cefepime; FOX, cefoxitin; CPD, cefpodoxime; CZ, cefazolin; MOX, moxalactam; IPM, imipenem; MEM, meropenem; ERY, erythromycin; TIL, tilmicosin; AZI, azithromycin; CHL, chloramphenicol; FFC, florfenicol; GEN, gentamicin; KAN, kanamycin; AMK, amikacin; SPT, spectinomycin; STR, streptomycin; NEO, neomycin; TOB, tobramycin; TET, tetracycline; DOX, doxycycline; OTC, oxytetracycline; MIN, minocycline; CIP, ciprofloxacin; LVX, levofloxacin; OFX, ofloxacin; ENO, enrofloxacin; MAR, marbofloxacin; DIF, difloxacin; OFX, ofloxacin; OBX, orbifloxacin; CL, colistin; CLI, clindamycin; VAN, vancomycin; S3, sulfonamides; SMX, sulfamethoxazole; TMP, trimethoprim; SXT, trimethoprim-sulfamethoxazole.

c

Resistance rates varied with incubation temperature (30°C or 37°C) and time (24 h or 48 h). Susceptibility data presented here were determined when isolates were incubated at 37°C for 24 h.

Available data are limited for the antimicrobial susceptibility of S. maltophilia, because it is not considered as a major pathogen in animals. However, S. maltophilia isolates from animals are resistant to numerous antimicrobials that are commonly used in human and veterinary medicine, including β-lactams (penicillins and cephalosporins), aminoglycosides, macrolides, and tetracyclines (except minocyline) (Table 2). In contrast, they are often susceptible to fluoroquinolones, polymyxins (mainly including polymyxin B and polymyxin E [colistin]), and SXT. The antibiotic resistance of S. maltophilia varies among different animal species. For example, one isolate from swine in China showed high resistance to most antimicrobials, including fluoroquinolones, polymyxins, and SXT (33), whereas isolates from Omani goats were susceptible to all tested antimicrobials except β-lactams (25). Despite its intrinsic resistance to β-lactams, the resistance rates of S. maltophilia isolates from captive snakes to these antimicrobials range from 36.2 to 95.7% (15, 37). Moreover, antimicrobial resistance varies with the incubation temperature and time. For instance, the MICs at 37°C and 30°C (after 24 h or 48 h) of 24 antibiotics were determined (microdilution method) for S. maltophilia isolates from captive snakes, but resistance rates increased when the strains were incubated at 30°C or for 48 h (37). However, SXT and levofloxacin were the most effective drugs at both temperatures. In addition, the S. maltophilia isolates from animal products also exhibit a multidrug-resistant (MDR) phenotype. For example, S. maltophilia was the most frequently isolated species among a large collection of Gram-negative bacteria isolated from milk and cheese in France. These S. maltophilia isolates showed high resistance rates to β-lactams, chloramphenicol, and tetracycline (13), representing a potential risk to food safety and public health.

MOLECULAR MECHANISMS OF ANTIMICROBIAL RESISTANCE

S. maltophilia employs an array of mechanisms that singularly or collectively, intrinsic or acquired contribute to antimicrobial resistance (Table 3). The following subsections provide detailed descriptions of the major mechanisms.

TABLE 3.

Molecular mechanisms of antimicrobial resistance of S. maltophiliaa

Resistance mechanisms and related genes Products Antibiotic resistance phenotype Intrinsic/acquired resistance Gene location Ref.
Multidrug efflux pumps
 smrA ABC-type efflux pump Fluoroquinolones, tetracycline, doxorubicin NK/yes C 38
 fuaABC ABC-type efflux pump Fusaric acid Yes/no C 41
 macABCsm ABC-type efflux pump Macrolides, aminoglycosides, polymyxins Yes/NK C 39
 emrCABsm MFS-type efflux pump Nalidixic acid, erythromycin No/yes C 40
 mfsA MFS-type efflux pump Aminoglycosides, cephalosporins, fluorpquinolones, erythromycin, rifampicin, tetracycline, chloramphenicol Yes/NK C 50
 smeABC RND-type efflux pump β-lactams, aminoglycosides and quinolones No/yes C 42
 smeDEF RND-type efflux pump Quinolones, tetracyclines, macrolides, chloramphenicol, novobiocin, SXT Yes/yes C 43, 53
 smeVWX RND-type efflux pump Chloramphenicol, quinolones, tetracyclines No/yes C 44
 smeIJK RND-type efflux pump Aminoglycosides, tetracyclines, fluorpquinolones, leucomycin Yes/yes C 46, 55
 smeYZ RND-type efflux pump Aminoglycosides, SXT Yes/yes C 45, 46, 54
 smeOP-TolCSm RND-type efflux pump Nalidixic acid, doxycycline, aminoglycosides, macrolides Yes/no C 47
β-lactamases
 blaL1 Metallo-β-lactamase β-Lactams except monobactams Yes/yes C or P 56, 97
 blaL2 Cephalosporinase Penicillins and cephalosporins Yes/yes C 57, 97
 blaTEM-2, blaTEM-116, blaTEM-127, blaCTX-M-1, blaSHV-1 and blaCTX-M-15 β-lactamase Penicillins and/or cephalosporins No/yes P 62–65
 blaNDM-1 Metallo-β-lactamase β-Lactams except monobactams No/yes C 66
Aminoglycoside-inactivating enzymes
 aac(6′)-Iz Aminoglycoside acetyltransferase Amikacin, netilmicin, sisomicin, tobramycin Yes/no C 67
 aph(3′)-IIc Aminoglycoside phosphotransferase Kanamycin, neomycin, butirosin, paromomycin Yes/no C 68
 aac(6′)-Iak Aminoglycoside acetyltransferase Amikacin, arbekacin, dibekacin, isepamicin, kanamycin, neomycin, netilmicin, sisomicin, tobramycin Yes/no C 69
 aac(6′)-Iam Aminoglycoside acetyltransferase NK NK C 45
Qnr family
 Smqnr Pentapeptide repeat proteins Low-level quinolone resistance Yes/no C 76–78
SXT resistance
 sul1 and sul2 Folate reductase enzyme Trimethoprim/sulfamethoxazole No/yes C or P 82–84
 dfrA1, dfrA5, dfrA12, dfrA17, and dfrA27 Dihydrofolate reductase enzyme Trimethoprim/sulfamethoxazole No/yes C or P 85
Phenicol exporters
 floR MFS exporter protein Chloramphenicol, florfenicol No/yes P 83
 floRv MFS exporter protein Chloramphenicol, florfenicol No/yes GI in C 33
 cmlA MFS exporter protein Chloramphenicol No/yes I-integron 90
Lipopolysaccharide
 spgM Phosphoglucomutase Polymyxin B/E, nalidixic acid, gentamicin Yes/NK C 92
 phoPQ Two-component regulatory system Polymyxin B, chloramphenicol, ampicillin, aminoglycosides Yes/yes C 96
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a

NK, not known.

Multidrug Efflux Pumps

The genome of S. maltophilia encodes multidrug efflux pumps, which contribute to intrinsic or acquired antibiotic resistance, as follows: ATP-binding cassette (ABC)-type (SmrA, FuaABC, and MacABCsm), major facilitator superfamily (MFS)-type (EmrCABsm, MsfA), and eight predicted resistance nodulation cell division (RND)-type efflux systems with SmeABC, SmeDEF, SmeVWX, SmeIJK, SmeYZ, and SmeOP-TolCSm characterized (38–47) and SmeMN and SmeGH uncharacterized (45). Most of the efflux pumps are superficially quiescent or expressed at low levels (39, 42, 44), and their overexpression is associated with reduced antibiotic susceptibility. Acquired resistance may be due to mutations in regulatory genes of these efflux systems (43, 46, 48).

SmrA, the first ABC-type efflux pump identified in S. maltophilia, confers acquired resistance to fluoroquinolones, tetracycline, doxorubicin, and multiple dyes (38). FuaABC, a fusaric acid (5-butylpicolinic acid, a mycotoxin) efflux pump, which is classified as a member of a subfamily of the ABC-type family, is induced by fusaric acid and contributes to fusaric acid resistance when overexpressed (41). The MacABCsm efflux pump confers intrinsic resistance to aminoglycosides, macrolides, and polymyxins and contributes to oxidative and envelope stress tolerance as well as biofilm formation (39). The MFS-type pump EmrCABsm is involved in the extrusion of hydrophobic compounds, including the antibiotics nalidixic acid and erythromycin, as well as the uncoupling agents carbonyl cyanide 3-chlorophenylhydrazone, and tetrachlorosalicylanilide (40). A novel MFS efflux pump (MfsA) with 14 transmembrane domains plays an important role in mediating resistance to paraquat (49), as well as to antibiotics such as aminoglycosides (kanamycin, streptomycin, and neomycin), cephalosporins (cefazolin and cefalexin), fluoroquinolones (ciprofloxacin, norfloxacin, levofloxacin, and ofloxacin), the macrolide erythromycin, rifampicin, tetracycline, and chloramphenicol (50).

SmeABC is involved in acquired, but not intrinsic, resistance to β-lactams, aminoglycosides, and quinolones. The deletion of smeC (encoding a porin) affects susceptibility to certain antibiotics, suggesting the relationship of porin to other unidentified efflux pumps (42). SmeDEF is involved in intrinsic and acquired (in the condition of overexpression) resistance to quinolones, tetracyclines, macrolides, chloramphenicol, novobiocin, and SXT, as well as acquired resistance to triclosan (51–53). SmeVWX mediates acquired resistance to chloramphenicol, quinolones, and tetracyclines and when overexpressed, increases susceptibility to aminoglycosides (44). SmeYZ mediates intrinsic resistance to aminoglycosides and SXT (45, 54), while SmeIJK is involved in intrinsic reduced susceptibility to gentamicin, amikacin, tetracycline, minocycline, ciprofloxacin, and leucomycin (45, 55). SmeIJK also mediated acquired resistance to levofloxacin, when overexpressed alone or in coordinate hyperproduction with SmeYZ (46). The activity of the SmeOP-TolCSm efflux pump is associated with the decreases in susceptibility to nalidixic acid, doxycycline, aminoglycosides (amikacin and gentamicin), and macrolides (erythromycin and leucomycin), as well as several nonantibiotic compounds including carbonyl cyanide 3-chlorophenylhydrazone, crystal violet, sodium dodecyl sulfate, and tetrachlorosalicylanilide (47).

Resistance to β-Lactam Antibiotics

The S. maltophilia genome encodes the inducible β-lactamases L1 and L2. L1 is a class B Zn2+-dependent metallo-β-lactamase with substrate preference for penicillins, cephalosporins, and carbapenems, except for monobactams; and L2 is a class A clavulanic acid-sensitive cephalosporinase that hydrolyzes penicillins, cephalosporins, and monobactams (56, 57). The expression of L1 and L2 is simultaneously regulated by AmpR, a transcriptional regulator encoded by ampR, located upstream of blaL2, which acts as a weak repressor or activator of the blaL2 in the presence or absence of β-lactam antibiotics, respectively (58). The induction of β-lactamases is inhibited by the deletion of the ampN-ampG operon, which encodes a permease transporter (59). The hyperproduction of L1/L2 β-lactamases occurs when the transcription of mrcA or ampDI (encoding penicillin-binding protein 1a [PBP1a] and a cytoplasmic N-acetyl-muramyl-l-alanine amidase [AmpDI], respectively) is inhibited (60, 61). In addition, the β-lactamases TEM-2, TEM-116, TEM-127, CTX-M-1, SHV-1, and CTX-M-15 and the globally disseminated metallo-β-lactamase NDM-1 are present in human clinical and environmental isolates of S. maltophilia (62–66), suggesting that this pathogen may serve as a reservoir for mobile genes that encode β-lactamases.

Resistance to Aminoglycosides

The mechanisms employed by S. maltophilia that mediate resistance to aminoglycosides primarily involve aminoglycoside-modifying enzymes and multidrug efflux pumps. These enzymes include the aminoglycoside acetyltransferase AAC(6′)-Iz (67) and the aminoglycoside phosphotransferase APH(3′)-IIc (68), both of which confer low-level resistance to aminoglycosides, with the exception of gentamicin. The novel aminoglycoside acetyltransferase AAC(6′)-Iak, which exhibits 86.3% amino acid identity to AAC(6′)-Iz, is expressed by an MDR S. maltophilia strain isolated from Nepal and acetylates amikacin, arbekacin, dibekacin, isepamicin, kanamycin, neomycin, netilmicin, sisomicin, and tobramycin, but not apramycin, gentamicin, or lividomycin (69). Moreover, AAC(6′)-Iam [84.3% amino acid sequence identity to AAC(6′)-Iak], was detected in a clinical isolate of S. maltophilia (45). However, the resistance phenotype conferred by this enzyme is unknown. In addition, the efflux pumps SmeABC, SmeYZ, SmeOP-TolCsm, and MacABCsm are associated with aminoglycoside resistance (Table 3).

Resistance to Quinolones

Mutations in the quinolone-resistance-determining region of genes encoding topoisomerases (gyrA, gyrB, parC, and parE) are associated with the major mechanism of quinolone resistance employed by bacteria (70). So far, mutations have not been detected in the quinolone-resistance-determining region of gyrA of S. maltophilia (71, 72). Amino acid residue substitutions are present in the quinolone-resistance-determining region-encoding regions of gyrB, parC, and parE of clinical isolates of S. maltophilia that cause bacteremia; however, these alterations have not been directly associated with quinolone resistance (73). The specific mechanisms associated with the quinolone resistance of S. maltophilia are mediated by both the efflux pumps and the chromosomal qnr gene (Smqnr) that protects gyrase and topoisomerase IV from quinolones (74). Smqnr and its functional 12 variants belong to the qnr family (75) and contribute to low-level intrinsic quinolone resistance (76–78). Genes that encode efflux pumps that mediate quinolone resistance are as follows: smeDEF, smeIJK, smeABC, and smeVWX (Table 3). The most prevalent cause of quinolone resistance in S. maltophilia is the overproduction of multidrug efflux pumps, among which the SmeDEF plays the most important role (79). Furthermore, overexpression of smeVWX in clinical isolates of S. maltophilia is associated with high-level resistance to quinolones (80).

Resistance to Trimethoprim-Sulfamethoxazole

The resistance of Gram-negative bacteria to sulfonamides is mainly conferred by the acquisition of either sul1 or sul2, encoding dihydropteroate synthases (81). The sul1 gene carried by class 1 integrons and sul2, which is linked to insertion sequence common region (ISCR) elements, was identified in SXT-resistant S. maltophilia isolates (82–84). The resistance of S. maltophilia to trimethoprim is mainly conferred by the dihydrofolate reductase dfr genes. For instance, the dfrA variant genes (dfrA1, dfrA5, dfrA12, dfrA17, and dfrA27), which are located within class 1 integrons as part of various resistance gene cassettes, are associated with high-level trimethoprim resistance in S. maltophilia isolates. Both types of sul and dfr genes can occur together in high-level SXT-resistant isolates (85, 86). Moreover, the efflux pumps SmeDEF, TolCsm, and SmeYZ are associated with SXT resistance (54, 87, 88).

Resistance to Phenicols

The main phenicol resistance determinant in S. maltophilia is floR, which encodes an exporter protein of the MFS family that mediates resistance to chloramphenicol and florfenicol (83). Florfenicol is extensively used in livestock to prevent or cure bacterial infections (89). In addition, the MFS exporter gene cmlA1 and chloramphenicol acetyltransferase genes catB2 and catB8, which separately reside in a gene cassette of class 1 integrons, confer resistance to chloramphenicol in S. maltophilia (82, 85, 90). Reports of the prevalence of floR in S. maltophilia are rare. One report that investigated an international collection of 55 clinical isolates of S. maltophilia found that four strains harbored floR (83). The novel variant floRv was detected in one porcine S. maltophilia isolate in China. The floRv gene encodes an exporter protein of 404 amino acids, which is 84.1 to 91.8% identical to FloR sequences deposited in GenBank. This FloR variant mediates resistance to chloramphenicol and florfenicol (33).

Alteration of Lipopolysaccharide and Two-Component Regulatory Systems

As in other Gram-negative bacteria, lipopolysaccharide (LPS) is an important structural component of the outer membrane of S. maltophilia and forms an effective barrier to exogenous compounds (91). The spgM gene encodes a phosphoglucomutase that is associated with LPS biosynthesis in S. maltophilia (92). Mutants lacking spgM, which produce less LPS compared with the SpgM+ strain, synthesize shorter O-polysaccharide chains and exhibit modest increases in susceptibility to polymyxin B, colistin, nalidixic acid, and gentamicin but increased resistance to vancomycin (92). The mobile colistin resistance gene mcr-1, which encodes a phosphoethanolamine transferase, couples phosphoethanolamine to the lipid A domain of the LPS component of the outer membrane of Gram-negative bacteria, and negates the efficacy of polymixins (93), has not been detected in Stenotrophomonas spp. The two-component regulatory system PhoPQ is involved in the resistance of numerous Gram-negative bacteria, including S. maltophilia, to cationic antimicrobial polypeptides, i.e., polymyxin B (94–96). Mutation of S. maltophilia PhoP increases susceptibility to polymyxin B, chloramphenicol, ampicillin, gentamicin, kanamycin, streptomycin, and spectinomycin (96). Moreover, downregulation of the SmeZ efflux transporter expressed by a PhoP mutant contributes to increased drug susceptibility, particularly to aminoglycosides (96).

DISSEMINATION, COSELECTION, AND PERSISTANCE OF RESISTANCE DETERMINANTS

As described above, the reduced susceptibility of S. maltophilia to most antibiotics can be attributed to intrinsic and acquired resistance. The proteins mediating intrinsic resistance of S. maltophilia include chromosomally encoded multidrug efflux pumps, antibiotic-inactivating enzymes (L1/L2 β-lactamases and aminoglycoside-inactivating enzymes), and the chromosomally encoded Qnr pentapeptide repeat proteins (74), which are present in most, if not all, strains of S. maltophilia, suggesting they did not arise during the recent evolution of resistance caused by antibiotic therapy. In addition, S. maltophilia can acquire mechanisms to increase its resistance through horizontal gene transfer via integrons, transposons, plasmids, and genomic islands (GIs). The sul1 gene is always associated with the class 1 integron in S. maltophilia, indicating the role of the latter in the acquisition and dissemination of sul1 within this species (82–86, 90). The qacEΔ1 gene, which encodes resistance to quaternary amines, coexists with sul1 at the 3′-termini of class 1 integrons (83, 85, 90). The gene cassettes, which comprise the variable regions of integrons, integrate different combinations of drug-resistance genes donated by other Gram-negative bacteria, including those encoding resistance to aminoglycosides [aacA4, aacA7, aadA1, aadA2, aadA4, aadA5, aadB, aac(6′)-II, aac(6′)-Ib, aac(3′)-Ia, and ant(3″)-Ia], trimethoprim (dfrA1, dfrA5, dfrA12, dfrA17 and dfrA27), β-lactams (blaCARB-8), rifampicin (arr-3), and chloramphenicol (catB2, catB8, cmlA1) (82, 85, 90).

ISCR elements are frequently associated with antimicrobial resistance genes and are always linked to sul2 in S. maltophilia. For example, seven sul2-positive S. maltophilia isolates harbor ISCR elements (five ISCR2 and two ISCR3 elements) on a plasmid (83). Moreover, sul2 and floR are linked to ISCR2 in all sul2-positive S. maltophilia isolates. Constitutively expressed blaTEM-2 resides within a novel Tn1/Tn3-type transposon in the genome of S. maltophilia isolate J675Ia (65). The transposon could mobilize blaTEM-2 onto the broad host-range conjugative plasmid R388, which is then transferred to E. coli.

The genes encoding β-lactamases L1 and L2 are invariably chromosomal and reside on an approximately 200-kb plasmid present in 10 clinical isolates of S. maltophilia (97). However, the sequences of the L1 and L2 genes diverge from that of the published strain IID 1275, indicating that the presence of β-lactamase genes on a plasmid may lead to their relatively quick evolution (97).

A literature search identified only a single report of an MDR GI in the S. maltophilia isolate GZP-Sm1 in China (33). GZP-Sm1 was isolated from swine with septicemia, and susceptibility testing revealed that the isolate was resistant to most antimicrobials employed in human and veterinary clinical practice (33). Whole-genome sequencing identified a GI of 40,226 bp, which contains an MDR region (19,364 bp) and is flanked by IS26 in opposite orientations (Fig. 1). Furthermore, six resistance genes exist in this region, including floRv (phenicol resistance), tet(A)-tetR (tetracycline resistance), strA/strB (streptomycin resistance), sul1 (sulfonamide resistance), and aadA2 (streptomycin/spectinomycin resistance). The MDR region comprises several segments with sequence similarity to plasmids or chromosomal sequences of other Gram-negative bacteria. For example, the aadA2 cassette and the 3′-CS region (qacEΔ1-sul1-Δorf5), which form part of an integron structure identified in this GI, occur in diverse bacterial species such as Salmonella spp., Pseudomonas spp., and E. coli. The 4,766-bp segment of Δsul-floRv-lysR-traG is 86.3% identical to the corresponding region of plasmid pAB (accession no. HQ917128) detected in a clinical isolate of Acinetobacter baumannii from Chile. The composite transposon comprising IS26-tet(A)-tetR-IS26 flanked by a direct repeat of GC is 95.1% identical to the corresponding region of the plasmid pB12 from uncultivable bacteria (accession no. JX469826). Inverse PCR showed that the GI could be excised from the chromosome by recombination between the direct repeats to generate a circular extrachromosomal form (Fig. 1). The emerging resistance of S. maltophilia to numerous antimicrobials raises the concern that the presence of resistance genes in the novel MDR GI drastically limit therapeutic options and may enhance their coselection when antimicrobials are administered.

FIGURE 1.

FIGURE 1

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Linear representation of the complete GI and its flanking regions in S. maltophilia GZP-Sm1. The regions in gray represent the flanking regions of the GI when inserted into the bacterial chromosome. The arrows indicate the directions of gene transcription, and truncated genes are indicated by rectangles without arrowheads. Genes are depicted in different colors, and the regions of particular relevance (≥95% nucleotide sequence identity) are indicated by the dotted lines (33).

S. maltophilia could acquire antibiotic resistance from Gram-positive bacteria. For example, a gene cluster involved in resistance to antibiotics and heavy metals was detected in a clinical isolate of S. maltophilia (98). These genes encode a macrolide phosphotransferase (mphBM) and a cadmium efflux determinant (cadA), as well as its transcriptional regulator (cadC), encoding its cognate transcriptional regulator. The cadC-cadA region is flanked by a truncated IS257 sequence and a region coding for a bin3 invertase. The sequences of these genetic elements are highly similar to those of Staphylococcus aureus, indicating their Gram-positive origin.

CONCLUSION

S. maltophilia is the most widely distributed environmental species among Stenotrophomonas, and it is also an opportunistic pathogen associated with the increased number of infections in both humans and animals. S. maltophilia isolates from animals are resistant to most antimicrobials used in both human and veterinary medicine, which compromise the design of optimal therapeutic strategies in clinical chemotherapy. The antimicrobial resistances in S. maltophilia are conferred not only by intrinsic mechanisms, but also by multiple acquired resistance mechanisms, which are commonly associated with mobile genetic elements such as integrons, transposons, and plasmids. Moreover, for the first time, the transmission mechanism conferred by MDRGI was identified in a porcine S. maltophilia isolate. Therefore, continued surveillance of MDR S. maltophilia from animals is warranted for not only optimizing treatment of infections caused by this bacterium, but also tackling the transmission of antimicrobial resistance from animals to humans by either food-chain or environmental routes.

ACKNOWLEDGEMENT

This work was supported in part by the National Natural Science Foundation of China (grant no. 31422055) and the National Key Basic Research Program of China (grant no. 2013CB127200).

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