10.1038@nrmicro2163

REVIEWS
The versatility and adaptation

of bacteria from the genus
Stenotrophomonas
Robert P. Ryan*, Sebastien Monchy‡, Massimiliano Cardinale§, Safiyh Taghavi‡,
Lisa Crossman||, Matthew B. Avison¶, Gabriele Berg§, Daniel van der Lelie‡ and
J. Maxwell Dow*
Abstract | The genus Stenotrophomonas comprises at least eight species. These bacteria
are found throughout the environment, particularly in close association with plants.
Strains of the most predominant species, Stenotrophomonas maltophilia, have an
extraordinary range of activities that include beneficial effects for plant growth
and health, the breakdown of natural and man-made pollutants that are central to
bioremediation and phytoremediation strategies and the production of biomolecules
of economic value, as well as detrimental effects, such as multidrug resistance, in
human pathogenic strains. Here, we discuss the versatility of the bacteria in the genus
Stenotrophomonas and the insight that comparative genomic analysis of clinical and
endophytic isolates of S. maltophilia has brought to our understanding of the adaptation
of this genus to various niches.
The genus Stenotrophomonas, which is phylogeneti‑ Although Stenotrophomonas spp. occur ubiquitously
cally placed in the Gammaproteobacteria, was first in the environment, soil and plants are their main
described with the type species Stenotrophomonas environmental reservoirs. S. maltophilia is a typical,
maltophilia 1 . This species was originally named often dominant member of the microbial communi‑
*BIOMERIT Research Centre,
Pseudomonas maltophilia by Hugh and Ryschenko ties that are found on or in plants and has a worldwide
Department of Microbiology, in 1961, but was later transferred to the genus distribution (reviewed in REFs 17,18). Members of the
BioSciences Institute, Xanthomonas 2 before it was given its own genus1. The genus Stenotrophomonas have an important ecological
University College Cork, genus name (from the Greek ‘stenos’, meaning nar‑ role in the nitrogen and sulphur cycles19–21 and several
Cork, Ireland.
row, ‘trophus’, meaning one who feeds and ‘monas’, Stenotrophomonas species, especially S. maltophilia
‡
Brookhaven National
Laboratory, Biology meaning unit) was intended to highlight the limited and S. rhizophila, can engage in beneficial interactions
Department, Upton, New York nutritional range of the bacterium1. However, several with plants (FIG. 1). S. maltophilia is also an emerging
11973‑5000, USA. studies subsequently demonstrated that the genus is human pathogen that is responsible for fatal infections
§
Institute for Environmental capable of great metabolic versatility and intraspecific in humans (reviewed in REFs 18,22). In contrast to the
Biotechnology, Graz
University of Technology,
heterogeneity 3–8 (FIG. 1) . The genus currently com‑ phylogenetically closely related genera Xanthomonas
Graz, Austria. prises eight species, S. maltophilia, Stenotrophomonas and Xylella, no Stenotrophomonas species are known to
||
Pathogen Sequencing Unit, nitritireducens 9 , Stenotrophomonas rhizophila 10 , be phytopathogenic (FIG. 2).
The Wellcome Trust Sanger Stenotrophomonas acidaminiphila11, Stenotrophomonas Various molecular tools, including transposon
Institute, Hinxton, Cambridge,
koreensis 12, Stenotrophomonas chelatiphaga 13, Stenotro mutagenesis, allelic exchange and reporter fusions,
CB10 1SA, UK.
¶
Department of Cellular and phomonas terrae 14 and Stenotrophomonas humi 14. have been developed to facilitate the genetic analy‑
Molecular Medicine, Stenotrophomonas dokdonensis was described in sis of the diverse activities of Stenotrophomonas spp.
University of Bristol, School of 2006 (REF. 15) but was transferred in 2008 to the genus Furthermore, the full genome sequence of an environ‑
Medical Sciences, University Pseudoxanthomonas 16. Phenotypic and genotypic mental isolate, S. maltophilia R551‑3, and a clinical
Walk, Bristol, BS8 1TD, UK.
Correspondence to R.P.R.
studies as well as analysis of the ecological and meta‑ isolate, S. maltophilia K279a, are now available. In this
e‑mail: r.ryan@ucc.ie bolic diversity of these bacteria have revealed further Review, we describe the versatility of bacteria from the
doi:10.1038/nrmicro2163 differentiation at the species level. genus Stenotrophomonas, using a comparison of these
514 | july 2009 | VoluMe 7 www.nature.com/reviews/micro
© 2009 Macmillan Publishers Limited. All rights reserved

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can produce extracellular enzymes (proteases, lipases,

OH nucleases, chitinases and elastases) that have been
shown to be important in plant colonization by other
O OH Cl rhizosphere microorganisms.
S. maltophilia produces various pili or fimbriae that
Biocontrol and plant have been implicated both in adhesion to surfaces33 and
growth promotion in the formation of complex biofilms. Both adhesion
Production of secondary Bioremediation and and biofilm formation might contribute to the ability of
metabolites phytoremediation S. maltophilia to compete with other microorganisms on
the surface of plant roots, and are certainly important
for the colonization of medical devices that leads to infec‑
Stenotrophomonas spp.
tion in humans34. de oliveira‑Garcia and colleagues33
characterized SMF1 fimbriae from S. maltophilia strains
SMDP92 and ATCC 1363. SMF1 fimbriae are com‑
posed of a 17 kDa fimbrin subunit that shares signifi‑
Pathogenesis of nematodes Hospital-acquired
infections cant amino‑terminal amino acid sequence similarity to
the CupA fimbriae of Pseudomonas aeruginosa and to
Figure 1 | Biotechnological uses of Stenotrophomonas spp. Stenotrophomonas spp.
Nature
have many traits that could be used in different biotechnological Reviews | Some
processes. Microbiology several fimbriae from pathogenic Escherichia coli.
Stenotrophomonas spp. can produce antimicrobial compounds that protect plants, as All of the clinical S. maltophilia isolates that were
well as generate factors that can promote plant growth. Also, many Stenotrophomonas tested produced the 17 kDa fimbrin. The genomes
spp. have a high level of intrinsic resistance to heavy metals and antibiotics and have of S. maltophilia strains K279a and R551‑3 con‑
been shown to degrade a wide range of compounds, including pollutants, and could tain genes that encode type I pili (Sterm_0582‑85,
potentially be used in bioremediation and phytoremediation. Stenotrophomonas Sterm_1304‑09 and Sterm_2358‑66; based on R551‑3
maltophilia is also known to cause human disease as a result of its ability to colonize genome annotation), which have been implicated in
immunocompromised patients, and has been shown to be virulent in a nematode model. adhesion and the early stages of biofilm formation, and
type IV pili (Sterm_1417‑22 and Sterm_3223–26), which
recently sequenced genomes to highlight the possible have been implicated in adherence, auto‑aggregation,
genetic basis of adaptation to different niches. twitching motility and biofilm formation. These gene
clusters are distributed throughout each genome of
Associations of Stenotrophomonas with plants the sequenced strains in a similar manner, which may
Stenotrophomonas species, especially S. maltophilia and indicate that there are some similarities in the plant
S. rhizophila, are often found in association with plants. and animal colonization strategies. Both S. maltophilia
These bacteria can be isolated from the rhizosphere23,24 SMDP92 and ATCC 1363 carry manA, manB, rmlB,
or from internal plant tissues, particularly from rmlA, rmlC and rmlD (also known as Stemr_0515‑30),
the vascular tissues of the root and stem ( FIG. 3 ; which encode enzymes involved in the biosynthesis of
Intraspecific heterogeneity
The quality of being diverse
Supplementary information S1 (movie)). Endophytic lPS and exopolysaccharides. Mutations in manA, rmlA
within a single species. strains of S. maltophilia have been isolated from the and rmlC affect biofilm formation and twitching motility
roots of many plant species, including cucumber in S. maltophilia WR‑C35.
Rhizosphere (Cucumis sativus)25, oilseed rape (Brassica napus)26, Epiphytic Stenotrophomonas bacteria can also alter
The zone around roots that
potato (Solanum tuberosum)26, strawberry (Fragaria the properties of the leaf surface to which they attach.
is influenced by the plant
and is a region of high
x ananassa)26, alfalfa (Medicago sativa)27, sunflower Schreiber et al.36 have demonstrated that S. maltophilia
microbial activity. (Helianthus annuus)27, maize (Zea mays)28, rice (Oryza Sao5sm can increase the water permeability of Hedera
sativa)29, wheat (Triticum astivum)30, various weeds, and Prunus cuticles, which in turn should increase the
Endophytic willow (Salix herbacea)31 and poplar (Populus)32. availability of water and dissolved compounds in the
A microorganism that lives
phyllosphere , thereby enhancing the environmental
within a plant for at least part
of its life cycle without causing Factors involved in plant colonization. Most Stenotro growth conditions for the bacteria. The molecular mech‑
apparent disease. phomonas spp. are highly adaptable to hostile and anism (or mechanisms) responsible for the observed
nutrient‑limited environments. Several factors have effects is as yet unknown, although it has been proposed
Epiphytic a known or suggested influence on the ability of that extracellular enzymes that degrade the cutin poly‑
Describes a bacterium that
grows on or attaches to the
Stenotrophomonas spp. to colonize and survive on plant mer and/or plasticizers, such as biosurfactants, could
surface of a living plant. surfaces. The establishment of interactions between be responsible37.
plants and microorganisms in the rhizosphere is pre‑ The synthesis of compatible solutes by bacteria con‑
Phyllosphere ceded by the movement of free‑living microorgan‑ tributes to their survival under the changing osmo‑
The micro-environment on
the leaf surface of a plant.
isms towards the plant roots and can involve chemotaxis larities that occur in the rhizosphere38. S. maltophilia
towards attractants that are present in plant root exu‑ accumulates trehalose as the only compatible solute,
Compatible solute dates. In addition to flagellar motility, other contributing whereas S. rhizophila produces glucosylglycerol in
An organic compound that factors to the colonization of plant tissues include a high addition to trehalose 39,40. These sugars often accu‑
acts as a cytoplasmic solute
bacterial growth rate, vitamin B1 synthesis, the exuda‑ mulate intracellularly and protect against various
to regulate water content
for bacterial cells growing
tion of NADH dehydrogenase and bacterial lipopolysac‑ stresses41. S. maltophilia K279a encodes the Smlt2757
in environments of high charides (lPSs), particularly the o antigen (reviewed in and Smlt2759 proteins, which are involved in the
osmolarity. REFs 17,18). Furthermore, many Stenotrophomonas spp. biosynthesis of trehalose through the degradation of
NATuRe ReVIeWS | MicroBiology VoluMe 7 | july 2009 | 515

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Pseudomonas trivialis DSM 14937T (AJ492831)

Pseudomonas fluorescens DSM 500 90T (Z76662)
Lysobacter spongiicola KMM329T (AB299978)
Xanthomonas campestris LMG 568T (X95917)
Pseudoxanthomonas broegbernensis B1616/1T (AJ012231)
75/ Pseudoxanthomonas mexicana AMX 26BT (NR_025105)

93
97/ Pseudoxanthomonas japonensis 12-3T (NR_024660)
100
Pseudoxanthomonas dokdonensis DS-16T (DQ178977)
Stenotrophomonas rhizophila e-p10T (AJ293463)
Stenotrophomonas koreensis TR6-01T (AB166885)
67/70
Stenotrophomonas acidaminiphila AMX 19T (NR_025104)
50/66
100/100
46/89 69/ Stenotrophomonas terrae R-32768T (AM403589)
93
70/ Stenotrophomonas humi R-32729T (AM403587)
55/60 97
Stenotrophomonas nitrireducens L2T (NR-025305)
Stenotrophomonas chelatiphaga LPM-5T (EU573216)
35/90 Stenotrophomonas maltophilia LMG958T (X95923)
Xylella fastidiosa GR.8935T (AF203391)
Xanthomonas melonis LMG 8670 (NR_026384)
40/60
Thermomonas fusca R-10289T (NR_025577)
66/75 Thermomonas haemolitica A50-7-3T (NR_025441)
Luteimonas mephitis B1953/27.1T (AJ012228)
70/84 Luteimonas marina FR1330T (EU295459)
Lysobacter antibioticus DSM 2044T (AB019582)
0.01 61/97 Lysobacter enzymogenes DSM 2043T (AJ298291)
Figure 2 | Phylogenetic analysis of the eight validly described Stenotrophomonas species and related taxa.
This neighbour-joining tree illustrates the maximum likelihood based on 16S rDNA sequences of Stenotrophomonas
species and related taxa. Bootstrap values for >50% of 100 replicates (maximum likelihood/neighbour joining) are
shown at the corresponding nodes. The scale bar represents 0.01 changes per nucleotide position.
glycogen by the Trey–TreZ pathway 42. Genes encod‑ are toxic to sensitive species of Paramecium43, a genus of
ing the enzymes in a second pathway for trehalose bio‑ unicellular ciliate protozoa that live in freshwater envi‑
synthesis that involves the conversion of maltose (the ronments. As similar rebA and rebB gene clusters are
trehalose synthase pathway), are carried on another found in Xanthomonas axonopodis pv. citri str. 306 and
region of the S. maltophilia K279a genome, which is in Shewanella denitrificans oS217, these proteins could
absent from S. maltophilia R551‑3 (Supplementary conceivably have a role in the defence of bacteria against
information S2 (table)). Both S. maltophilia K279a and predation by protozoa in the rhizosphere or bulk soil.
S. maltophilia R551‑3 can also produce trehalose from
glucose through the trehalose‑6‑phosphate synthase– Biotechnological uses of Stenotrophomonas spp.
trehalose‑6‑phosphate phosphatase pathway (encoded Stenotrophomonas spp. are promising candidates for
by otsA and otsB). However, unlike the clinical iso‑ biotechnological applications in agriculture; treatment
late S. maltophilia K279a, the environmental isolate with Stenotrophomonas spp. can result in enhanced plant
R body S. maltophilia R551‑3 does not encode the pathway to growth and can influence plant development on marginal
A bacterial inclusion use trehalose and therefore cannot use this sugar as a soil (FIG. 1). For example, plant growth promotion of up
consisting of long sole carbon source32. to 180% was observed for wheat, tomato, lettuce, sweet
proteinaceous ribbons rolled
S. maltophilia might also have the capacity to protect pepper, melon, celery and carrot in the highly salinated
up inside the bacterial cell.
itself from predation by soil protozoa, which could confer soils of uzbekistan17. Stenotrophomonas spp. also have
Phenolic compound a selective advantage over other bacteria. The genome of promising applications in bioremediation and phytore‑
A chemical compound that is the environmental isolate S. maltophilia R551‑3 contains mediation44, as these bacteria can metabolize a large range
characterized by the presence a cluster of six genes (Stemr_2139‑44), which is absent of organic compounds that are present in the rhizosphere,
of a hydroxyl group attached
to a six-membered aromatic
from the S. maltophilia K279a isolate (Supplementary including phenolic compounds found in plant root exudates.
ring; many plants produce information S3 (table)). The rebA–C genes encode Accordingly, S. maltophilia can degrade p‑nitrophenol and
phenolic compounds. refractile inclusion bodies, known as R bodies, which 4‑chlorophenol45, polycyclic aromatic hydrocarbons46,

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a b d f
c e g
Figure 3 | root and endosphere colonization by Stenotrophomonas rhizophila. Volume renderings of confocal
Nature Reviews | Microbiology
laser scanning micrographs of DsRed-labelled Stenotrophomonas rhizophila DSM 14405T cells in the rhizosphere of
tomato plants. a | Colonization of 1-week-old tomato roots. The colonization pattern is characterized by small colonies
that mainly grow inside the epidermal cells and the root hairs. b,c | Magnifications of the regions selected by the
continuous line and dotted line, respectively, in part a, observed from a different angle. d | Seven S. rhizophila DSM
14405T cells forming a cluster inside a new tomato root hair. e–g | Cutting planes of the image in panel d on the x, y and z
axes, respectively. The scale bars represent 40 μm (a), 3 μm (b), 20 μm (c) and 5 μm (d–g). Images courtesy of C. Zachow,
Graz University of Technology, Austria.
selenium compounds47, benzene, toluene, ethylbenzene48 Biocontrol properties. The potential of Stenotrophomonas
and xenobiotics44,48. These broad metabolic properties spp. for the biocontrol of oomycete, fungal and bacterial
could provide plants with protection against the phyto‑ pathogens has been demonstrated in several systems
toxic effects of these compounds. Stenotrophomonas spp. that include both monocotyledonous and dicotyle‑
can enhance plant productivity by several mechanisms, donous crops as hosts53–61 (examples of these are pro‑
including the production of the plant growth hormone vided in TABLE 1). Stenotrophomonas spp. can prevent
indole‑3‑acetic acid (IAA)49, nitrogen fixation21,50 and the the growth or activity of plant pathogens by several
oxidation of elemental sulphur, which in turn provides sul‑ different mechanisms. In vitro, most S. maltophilia iso‑
phate for the plants19. examples of how Stenotrophomonas lates have antifungal activity 7, and the new antifungal
spp. have been used in such applications are provided in compounds maltophilin62 and xanthobaccin60 have
TABLE 1. In the following sections, we detail some of the been described. Stenotrophomonas spp. also produce
traits of Stenotrophomonas spp. that make them amenable volatile organic compounds (VoCs) with antifungal
to such applications. activity 63–65 (see below). S. maltophilia strains have an
extraordinarily high hydrolytic potential; they pro‑
Metal tolerance. Many S. maltophilia strains have intrin‑ duce diverse proteases, chitinases, glucanases, DNases,
sic resistance to various heavy metals51,52. For example, RNases, lipases and laccases23,66,67. Both chitinolytic
the S. maltophilia strains Sm777 and D457R have been and proteolytic activities contribute to the biocon‑
shown to tolerate various toxic metals, such as cadmium, trol activity of S. maltophilia 61,68–70. Chitinases might
lead, cobalt, zinc, mercury and silver. When tested in protect plants against fungal pathogens through fun‑
tenfold diluted tryptic soy broth, strain Sm777 is addi‑ gal cell wall lysis but might also have a role in trig‑
tionally tolerant to 50 mM selenite, 25 mM tellurite and gering plant defence mechanisms71. A chitinase from
50 mM uranyl salts. These properties of S. maltophilia S. maltophilia strain C5 was shown to suppress summer
have the potential to be exploited for bioremediation patch disease (caused by Magnaporthe poae lanschoot
purposes or to aid phytoremediation. Furthermore, the and jackson) in Kentucky bluegrass by the activation of
tolerance of S. maltophilia strains to heavy metals could disease resistance genes72. The precise roles of the other
be useful in the bioremediation of soils that are polluted exoenzymes in the antagonistic activity of S. maltophilia
Xenobiotic
with heavy metals and xenobiotics. remain to be elucidated and it is therefore likely that
A chemical that is only A different complement of genes that specify metal further bacterial products also control plant disease by
man-made, and otherwise is tolerance has been identified in the S. maltophilia inducing plant defences.
not found in the environment. R551‑3 and K279a genomes (Supplementary informa‑ Another factor that is important for the con‑
tion S4 (table)). Genes coding for copper and mercury trol of fungal infection is competition for iron.
Biocontrol
The control of harmful pests resistance, located on a genomic island in S. maltophilia Stenotrophomonas cells can efficiently capture
and pathogens through the K279a, were absent from the S. maltophilia R551‑3 siderophores that are produced by other microorgan‑
use of microorganisms. genome. Conversely, loci coding for arsenic resist‑ isms 73, such as ferrichrome, which is produced by
ance (ars, Stemr_2020‑2024) and two tellurium resist‑ fungi of several genera, including the phytopatho‑
Siderophore
A small organic molecule
ance proteins (Stemr_2893‑94) were identified in the genic genus Ustilago 74. Both of the sequenced S. mal
that is produced by bacteria S. maltophilia R551‑3 genome but were absent from tophilia genomes encode many TonB‑dependent
to sequester iron. the S. maltophilia K279a genome. receptors (TBDRs), outer membrane proteins that

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Table 1 | Applications of Stenotrophomonas spp. in biocontrol VOCs. The VoCs that are produced by Stenotrophomonas
spp. can also negatively influence fungal growth and
Strain Pathogen and/or plant species refs serve as inter‑ and intra‑organismic communication
Stenotrophomonas maltophilia Soil-borne pathogen 55 signals64,65. Many different VoCs that are produced by
S. maltophilia Rhizoctonia solani damping-off in bark 58 S. maltophilia and S. rhizophila inhibit mycelial growth
compost media of the soil‑borne pathogen Rhizoctonia solani by more
S. maltophilia 3089 Verticillium dahliae; oilseed rape 54 than 90%63. Two of these VoCs have been characterized
as β‑phenylethanol and dodecanal. The precise mode
S. maltophilia 34S1 Summer patch disease of turf grass 57,72
of action of these secondary metabolites on the target
S. maltophilia C3* Biocontrol of brown patch disease 56 organism is not known. By contrast, VoCs such as ace‑
Stenotrophomonas sp. strain SB-K88 Sugar beet damping-off disease 60 tone, 2‑methyl‑1‑butanol, heptanal and octanal, which
S. maltophilia C3* Bipolaris sorokiniana; tall fescue 61 are produced by Trichoderma spp., are known to reduce
fungal growth by inhibiting protein synthesis78.
S. maltophilia W81 mutant with Biological control of Pythium ultimum 54
overproduction of an extracellular
serine protease Antimicrobial resistance
Many strains of S. maltophilia are also well known for
S. maltophilia 18 Fusarium graminearum; wheat 155
their multiple antibiotic resistance phenotypes7, which
S. maltophilia RAY132 Sulphur-oxidizing PGPR; canola 19 is consistent with the elevated antibiotic and bacteri‑
S. maltophilia PD3533 Ralstonia solanacearum race 3 biovar 2; 59 cidal selection pressure that is found in their biotopes79.
potato Multiple antibiotic resistance could help S. maltophilia to
S. maltophilia R551-3 Endophytic strain isolated from poplar 32 compete in the rhizosphere3,79,80, which supports intense
*In a series of papers, the potential of S. maltophilia to control plant pathogens was microbiological activity and competition in comparison
described56,61. Later, a taxonomic study published by Sullivan et al. showed that this strain to the nutrient‑limited bulk soil. Comparative genomic
belongs to Lysbacter enzymogenes156. PGPR, plant growth promoting rhizobacteria. analysis and experimental testing of the clinical and
endophytic S. maltophilia isolates K279a and R551‑3
are primarily known for the active transport of showed that many of the genes that encode antimicro‑
iron–siderophore complexes in Gram‑negative bac‑ bial drug resistance and resistance‑nodulation‑division
teria. In Xanthomonas campestris, different subsets (RND) family transporters (tripartite efflux pumps
of TBDRs mediate iron uptake and the use of plant that are involved in antibiotic resistance) are conserved
carbohydrates75. There are major differences, however, (Supplementary information S4 (table)). In addition,
in the complement of genes encoding TBDRs; the the S. maltophilia R551‑3 genome carries two additional
S. maltophilia R551‑3 genome carries 82 such genes RND operons (Stemr_2065‑67 and Stemr_951‑52) that
compared with 65 in the S. maltophilia K279a genome. are putatively involved in antibiotic efflux, a macrolide
Many of the genes that are present in S. maltophilia ATP‑binding cassette‑type transporter (Stemr_2509‑10)
R551‑3 but absent from S. maltophilia K279a are and three putative major facilitator superfamily anti‑
linked to genes encoding proteins that are involved in biotic transporters (Stemr_3598, Stemr_3605 and
iron transport and siderophore uptake. Such an over‑ Stemr_3603, the last of which is putatively involved
representation of TBDRs is found in only a limited in chloramphenicol transport). The presence of these
number of organisms, but is common in Xanthomonas genes indicates that the endophytic and clinical strains
spp. and in aquatic bacteria that scavenge complex car‑ have a similar level of antibiotic resistance, with possibly
bohydrates75. Although both S. maltophilia R551‑3 and an even broader resistance spectrum for the endophytic
K279a produce the siderophore enterobactin, this strain S. maltophilia R551‑3. In both strains, most anti‑
additional capacity for iron uptake suggests that iron biotic resistance genes are not associated with mobile
competition with other organisms for endophytic (or genetic elements, such as phages or transposons, which
rhizospheric) growth is important. makes it unlikely that S. maltophilia K279a acquired its
antibiotic resistance genes in the clinical environment.
Bioactive natural products. Many plant‑associated bac‑
teria are well known for their diverse range of secondary Adaptation and metabolic versatility
metabolic products, including antibiotics, anticancer Stenotrophomonas spp. can efficiently colonize such dif‑
compounds, VoCs and antifungal, antiviral, insecti‑ ferent biotopes as plants, humans and marine environ‑
cidal and immunosuppressant agents. S. maltophilia ments. Comparative studies of the recently determined
strains also produce bioactive compounds, including genome sequence of the endophytic S. maltophilia strain
antibiotics and enzymes76,77. Several proteases produced R551‑3 with that of the clinical isolate S. maltophilia
by Stenotrophomonas spp. are so much more effective K279a have provided insight into functions that could
than those currently in use in industry that it is thought be associated with adaptation to these different niches.
these proteases could ‘revolutionize’ washing agents78. Approximately 85% of the 4,175 S. maltophilia R551‑3
A selection of these compounds has been highlighted genes are homologous to genes from S. maltophilia
in BOX 1. Although a wide range of biologically active K279a, and have the same organization in both strains
Biotope compounds has been isolated from Stenotrophomonas (FIG. 4). This indicates that the ancestral S. maltophilia
The natural environment of a spp., these organisms still remain an untapped source core genome had to be well equipped to allow survival,
microorganism. of novel natural products. colonization and competition for resources in such a

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Box 1 | Stenotrophomonas species as a source of useful compounds and activities

Stenotrophomonas spp. have promising applications in bioremediation and phytoremediation44 as a result of their ability to
metabolize many of the compounds that are present in the rhizosphere, including xenobiotics. A selection of the xenobiotic
compounds that Stenotrophomonas spp. can degrade is provided in the table. Strains of Stenotrophomonas maltophilia could
be exploited in the bioremediation of polluted soils owing to their intrinsic resistance to heavy metals. Stenotrophomonas
spp. are also capable of biocatalysis, including the conversion of linoleic acid to 10-hydroxy-12(Z)-octadecenoic acid.
Useful compound or activity refs

Degradation of xenobiotic compounds
Biodegradation of p-nitrophenol, 4-chlorophenol and 4-nitroaniline 139
N-demethylation of the insecticide acetamiprid 140
Biodegradation of nonylphenol 141
Degradation of polypropylene glycols 142
Decolourization of synthetic dyes 67
Degradation of keratin 143
Degradation of herbicides 4-(2,4-dichlorophenoxy) butyric acid and 4-(4-chloro-2-methylphenoxy) butyric 144
acid
Heavy metal tolerance and remediation
Accumulation of intracellular uranium 145
Tolerance of heavy metals 52
Removal of Au(III) from contaminated waste water 146
Cr(VI) resistance 147
Biocatalysis and synthesis of novel compounds
Conversion of linoleic acid to 10-hydroxy-12(Z)-octadecenoic acid 148
7α-OH epimerization of bile acids 149
Hydroxysteroid dehydrogenase 150
Cholylglycine hydrolase 150
Aminopeptidase activity against 4-hydroxyproline-containing peptides 151
Synthesis of glucosylglycerol 39
Saccharification of alginate 152
Synthesis of terephthalic acid 153
Production of the glycosidase inhibitor valienamine from validomycin A 154
Biocontrol and antimicrobial activity
Production of antifungal xanthobaccins and the macrocyclic lactam antibiotic maltophilin 23,61
wide range of biotopes. Divergence in the gene com‑ insertion hotspots in the core genome of this species
plement of the two organisms might reflect adaptation (FIG. 5). In addition to genomic islands, the S. maltophilia
to specific niches, and in the following sections we R551‑3 genome carries 14 complete insertion sequence
highlight some of these differences. (IS) elements: five intact copies of the IS481 family, three
The S. maltophilia R551‑3 genome contains 27 intact copies of the IS3 (also known as IS150) family
regions that are absent from S. maltophilia K279a; (identical to ISPsy9 from K279a) and six intact copies of
the size of these regions ranges from 1.7 kb to 61.5 kb the IS110 family. Two additional truncated transposases
(Supplementary information S2,S3 (tables)). Six of of the IS110 family were also identified. In addition, two
these regions represent putative genomic islands, as phages were found, one of which (Stemr_910‑36) also
characterized by different codon usage from the rest of occurs in S. maltophilia K279a.
the genome, location next to a tRNA gene and/or the Filamentous haemagglutinin proteins are adhesins
presence of a flanking integrase gene. By contrast, the that are secreted by the type V protein secretion pathway
genome of S. maltophilia K279a contains 19 regions that and are involved in cell–cell aggregation. These filamen‑
are absent from S. maltophilia R551‑3 (Supplementary tous haemagglutinins have also been shown to mediate
information S2,S3 (tables)), five of which are putative contact between the phytopathogen Xylella fastidiosa
genomic islands80. These islands are often inserted at the and plant cells81 and are important virulence factors
same positions in both the S. maltophilia R551‑3 and that are involved in the adhesion of Bordetella pertus
K279a genomes, which points to the existence of sis to mammalian host cells82. S. maltophilia R551‑3

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4,500 kb 0 kb b 0 kb
a 4,500 kb
500 kb
4,000 kb 500 kb
4,000 kb
1,000 kb
1,000 kb
3,500 kb S. maltophilia S. maltophilia
R551-3 K279a
3,500 kb
1,500 kb
1,500 kb
3,000 kb
3,000 kb
2,000 kb 2,000 kb
2,500 kb
2,500 kb
Figure 4 | genome maps of Stenotrophomonas maltophilia r551‑3 and K279a. Genome maps of the poplar
endophyte S. maltophilia R551-3 (a) and of the opportunistic pathogen S. maltophilia K279a (b) are shown. From the
Nature
outside in, the circles represent coordinates in kilobase pairs (kbp),%GC content, Reviews
predicted | Microbiology
open reading frames (ORFs)
in the clockwise and anticlockwise orientations, GC skew ((G–C and G+C) in a 1,000-bp window), transposable elements
(pink) and pseudogenes (grey), and the putative S. maltophilia K279a genomic islands (red).
encodes three filamentous haemagglutinins (Stemr_0113, Variation in lPS biosynthetic gene clusters between
Stemr_2248 and Stemr_2356). one of these (Stemr_0113) strains is common in bacterial pathogens of animals, for
has a low level of amino acid sequence similarity (only which it might have a role in evading the host immune
53% identity) with its S. maltophilia K279a homologue system. The role of differences in o antigen or lPS
(shlA, which encodes Smlt1390) compared with the aver‑ structure between related plant pathogenic or plant‑
age similarity of proteins that are shared by the two strains. associated bacteria is less certain, although involve‑
The S. maltophilia K279a haemagglutinin is located with ment in host‑range selection and specificity has been
five haemagglutinin open reading frame fragments. proposed87. Serotype analysis of a range of S. maltophilia
Another region that is specific to S. maltophilia K279a strains, however, shows no clear delineation between
and is located on a putative complex transposon carries clinical and environmental isolates. Furthermore, other
genes that encode an adhesin and a type IV pilus as well roles for variations in o antigen structure, such as pro‑
as a peptidase (Supplementary information S2 (table)). moting insensitivity to phage infection, should not be
All these differences between S. maltophilia K279a and overlooked.
S. maltophilia R551‑3 could be related to niche adaptation The endophytic strain S. maltophilia R551‑3, which
or host preference. has no direct plant growth promoting effects on its
A key component of the bacterial outer membrane is poplar host, does not carry genes for the plant growth
lPS, and changes in lPS structure have been correlated promotion mechanisms that have been described for
with changes in resistance to various antimicrobial agents. other endophytes, such as metabolism of the plant
Many studies have examined the lPS in S. maltophilia in signal molecules γ‑amino butyric acid and phenyl
an effort to assess its contribution to antimicrobial resist‑ acetic acid, degradation of the ethylene precursor
ance in this organism83,84 and as a basis for serotyping. 1‑aminocyclopropane‑1‑carboxylic acid and acetoin
As outlined above, mutations in manA, rmlA and rmlC production. In addition, only low levels of IAA are
affect lPS structure in S. maltophilia WR‑C35. Adjacent produced by S. maltophilia R551‑3 (REF. 32).
to these genes in the sequenced genomes is a locus that Although S. maltophilia is related to plant patho‑
is also probably involved in lPS biosynthesis and that genic Xanthomonas spp., it is not a phytopathogen and
shows considerable variability between the two S. mal accordingly neither the S. maltophilia K279a nor R551‑3
tophilia strains (Supplementary information S5 (figure)). genomes encode genes that are known to contribute
This locus is flanked by the genes encoding cystathionine to Xanthomonas virulence, including those encoding
gamma lyase (metB) at one end and an electron transport the type III secretion system and genes encoding cer‑
flavoprotein (etfA) at the other. An equivalently located, tain plant cell wall degrading enzymes, such as pecti‑
highly variable lPS locus has been described in a range nases. These sequences also do not seem to encode the
of xanthomonads that infect rice, citrus and crucifers85 virulence factor type VI secretion system. In addition,
and was probably acquired by horizontal gene transfer 85. neither genome carries the zonula occludens toxin (zot)
Differences in the complement and nature of the genes gene that was identified in several clinical isolates of
in this locus are indicative of alterations in the structure S. maltophilia88. This gene is similar to the zot gene in
of lPS, particularly the o antigen moiety. Serotyping of Vibrio cholerae, which encodes the major virulence fac‑
heat‑stable o antigens from S. maltophilia has revealed tor enterotoxin88. However, genes that are involved in
a considerable level of variation between isolates, with phytopathogenesis, including those encoding enzymes
31 defined serotypes. The structure of the o antigen such as cellulase (glycosyl hydrolase family 5) and those
polysaccharides has been described for a number of these encoding type I, type II (Sec), type IV, type V and the
serotypes. Most of the polymers have branched repeating twin arginine transporter (TAT) secretion systems,
units, often with lateral pentosyl substitutions86. are present. Functional genomic analysis will allow an

REVIEWS
O antigen and Restriction and/or Phage and Glycosyl Chloramphenicol

cell wall biogenesis methylation macrolide hydrolases transport, peptidoglycan
transporter synthetase and
Putative nucleoside Colicin glutathione-S-transferase
Tellurite
triphosphate hydrolases Phage transport resistance
S. maltophilia
R551-3
S. maltophilia
K279a
ISXac3 and Phage
Phage cluster 1 Putative cell surface
smmJ, K and L
Potential haemagglutinin
conjugative Complex transposon
Intact phage Haemagglutinin insertion
cluster 2 transposon and/or
haemolysin
Glycosyltransferase and
LPS O antigen biosynthesis
Figure 5 | comparison of gene content and organization in the genomes of Stenotrophomonas maltophilia
r551‑3 and K279a. The genomes were compared using LinePlot from MaGe (see Nature
FurtherReviews | Microbiology
information). Syntenic regions
between S. maltophilia R551-3 and K279a are displayed in purple, and the location and putative functions of selected
genes within regions that are specific to each strain are indicated. The green boxes represent putative genomic islands
whereas the blue boxes represent virulence genes. LPS, lipopolysaccharide.
investigation of the factors that are important for the Hela cell lines after 24 hours101, and S. maltophilia K279a
association of Stenotrophomonas spp. with plants. killed almost all of the N2 Caenorhabditis elegans in the
assay within 24 hours102. However, as one might expect
S. maltophilia: an opportunistic pathogen of a true opportunist, S. maltophilia has no type III
S. maltophilia is the only species of Stenotrophomonas secretion system80.
that is known to cause human disease 5, but there is A recent study by Waters and colleagues103 tried to
considerable phylogenetic and phenotypic variability address the lack of documentation of the potential of
among S. maltophilia isolates, including those from S. maltophilia for virulence by investigating the immuno‑
patients in a single hospital89–91. This is probably the stimulatory properties of 24 S. maltophilia clinical res‑
result of the many environmental niches of this bacte‑ piratory and non‑respiratory isolates (from blood, skin
rium; most infections are likely to reflect contact with and soft tissue). In this study, which involved a neonatal
separate environmental sources. Indeed, there are few mouse model of pneumonia and macrophage cell lines,
instances of outbreaks of S. maltophilia, and those that they determined the rates of pneumonia, bacteraemia
occur are caused by a single contaminated source, such and mortality, as well as the inflammatory response that
as a water source92–95. Despite this, there is evidence is elicited by S. maltophilia infection. They demonstrated
that certain phylogenetic groups are better able to cause that the respiratory and non‑respiratory S. maltophilia
infection than others96. isolates were highly immunostimulatory but weakly
S. maltophilia is almost exclusively a hospital‑ invasive, which indicates that these isolates could
acquired pathogen and has been associated with bacter‑ contribute to airway inflammation.
aemic infections and pneumonia, both with a high rate Whether S. maltophilia clinical isolates are coloniz‑
of mortality 97, in immunocompromised patients. This ers or true pathogens is still controversial in some cases.
reflects a requirement for three major risk factors for This is particularly the case for pneumonia, because it is
infection: severe debilitation and/or neutropenia; the rare to culture pure S. maltophilia from the lungs, and
presence of indwelling devices such as ventilator tubes severely debilitated patients are often colonized asymp‑
and/or intravenous catheters for prolonged periods; and tomatically 104,105. Nonetheless, a recent study showed
multiple and/or prolonged courses of broad‑spectrum that 4.5% of nosocomial pneumonia in patients in inten‑
antimicrobial drugs98–100. There are also examples of sive care units and 6% of ventilator‑associated pneu‑
soft tissue, ocular, wound and burn infections, and monias are caused by S. maltophilia106. The attributable
endocarditis18. mortality for S. maltophilia pneumonia (as far as this
The bacteraemia isolate S. maltophilia K279a carries can be accurately quantified in patients with multiple
several genes that encode factors that could allow this and complex pathologies) is estimated at 20–30%107. As
strain to adhere to surfaces and form biofilms, which many as 25% of adult patients with cystic fibrosis carry
are both key factors in the colonization of indwelling S. maltophilia in their lungs at any one time, although
devices. Studies have shown that S. maltophilia isolates these numbers are highly variable108. Also, there is no
have cytotoxic effects in vitro against Hep‑2, Vero and evidence of any reduction in lung function associated

REVIEWS
with S. maltophilia colonization109. Although the rates with cystic fibrosis, where S. maltophilia can protect anti‑
are variable, approximately 1% of all nosocomial bacter‑ biotic‑sensitive strains of P. aeruginosa by degrading anti‑
aemias are caused by S. maltophilia and the attributed biotics132. Interspecies signalling between these organisms
mortality has been estimated at approximately 25%110. can also influence P. aeruginosa. S. maltophilia possesses a
These bacteraemias are usually caused by an indwelling cell–cell signalling system that is mediated by a diffusible
device, and the prognosis is usually good following the signal factor (DSF) that was first identified in the related
removal of the device111–113. plant pathogen X. campestris102,133. In S. maltophilia strain
The primary reason for the increase in S. maltophilia WR‑C the DSF can be one of eight structurally related
infections is the intrinsic resistance of this species to fatty acids that include cis‑11‑methyl‑2‑dodecenoic acid,
many front‑line antimicrobials, such as β‑lactams, the DSF signal from X. campestris133,134. Genome analyses
including carbapenems114, aminoglycosides (except revealed that S. maltophilia does not synthesize N‑acyl
gentamicin)48,80,115,116, macrolides, tetracycline, chloram‑ homoserine lactones (N‑AHls) or autoinducer 2 (AI2),
phenicol and older quinolones80,117–119. Furthermore, which are signal molecules that are commonly found in
S. maltophilia isolates can rapidly develop resistance to other Gram‑negative organisms, and N‑AHls have not
newer fluoroquinolones, gentamicin and minocycline been detected in S. maltophilia cultures135,136. In the clini‑
through mutation; the underlying mechanisms are not cal isolate S. maltophilia K279a, DSF signalling controls
certain, but are likely to be the result of the overproduc‑ several functions, including the production of an extra‑
tion of intrinsic efflux pumps89. Typically, empiric therapy cellular protease, aggregative behaviour and virulence in
for S. maltophilia is trimethoprim–sulphamethoxazole a nematode model102. Although P. aeruginosa does not
(TMP–SMX), to which >95% of isolates are sensitive120,121. synthesize DSF, it can respond to the signal that is pro‑
However, resistance is increasing as a result of the spread duced by S. maltophilia by altering biofilm architecture
of acquired mobile resistance determinants122,123 and, in and increasing tolerance to the cationic antimicrobial
many patients, TMP–SMX therapy is contra‑indicated124. peptides polymyxin B and colistin137,138. This response
Alternatives include ticarcillin–clavulanate, respiratory of P. aeruginosa to DSF requires PA1396, a sensor kinase
quinolones such as gatifloxacin and moxifloxacin, mino‑ with an input domain that is related to the sensory input
cycline and possibly tigecycline120,125. For how long these domain of RpfC, which is responsible for DSF percep‑
drugs would remain clinically efficacious if they were tion in xanthomonads. Homologues of PA1396 occur in
used as front‑line therapy is uncertain, however, as resist‑ other pseudomonads, some of which are plant patho‑
ant mutants arise spontaneously at high rates in vitro96 genic or plant associated, as well as in unrelated bacte‑
(V. C. Gould and M.B.A., unpublished observations). ria, including the poplar endophyte Enterobacter sp. 638.
The de novo mobilization of antibiotic resistance These observations indicate that modulation of bacterial
genes from environmental bacteria or opportunistic behaviour through DSF‑mediated interspecies signal‑
pathogens has contributed greatly to the increase in ling with S. maltophilia is a phenomenon that could also
antibiotic resistance in more common and important occur in a non‑pathogenic context in rhizospheric or
pathogens. examples include the mobilization of the endophytic communities.
SHV and CTXM β‑lactamase genes from Klebsiella
pneumoniae and Kluyvera spp., respectively, on com‑ Implications for biotechnological uses. The application
posite transposons that are likely to have formed since of rhizospheric and endophytic S. maltophilia strains to
the clinical use of antibiotics began126,127. one potential control plant pathogens59 or promote plant health should
consequence of the increased colonization of patients be carefully considered. Not only do these strains present
by S. maltophilia is the mobilization of its l1 metallo‑ a risk as reservoirs for antibiotic resistance genes, but
β‑lactamase gene onto a plasmid that can then confer they also have potential as opportunistic pathogens. It is
broad‑spectrum β‑lactam resistance, including to the known that clinical isolates of S. maltophilia and other
last‑line carbapenems, in P. aeruginosa and even the opportunistic pathogens can actively multiply in the
enterobacteriaceae. Another possibility is the mobili‑ rhizosphere49. This has led to suggestions that the rhizo‑
zation of a potential quinolone resistance determinant, sphere is an environmental reservoir for such opportun‑
qnr, that was identified in the S. maltophilia K279a128 and ists. Furthermore, the mechanisms responsible for the
R551‑3 genome sequences (Supplementary information colonization of plants and for the antagonistic activity
S4 (table)). Resistance plasmid and transposon carriage of S. maltophilia strains against plant pathogens are
has been demonstrated in S. maltophilia, as has sharing of similar to those that are responsible for the colonization
these elements with E. coli in vitro123,129–131, suggesting that of human tissues and for pathogenicity 79. Such consid‑
it might be only a matter of time before l1 mobilization erations should perhaps be translated into appropriate
occurs, which would be a hugely significant event. measures, such as banning plants from hospitals.
Polymicrobial infections and interspecies signalling. Concluding remarks

There is an increasing appreciation of the polymicrobial A fuller understanding of the versatility, adaptation
nature of human infections and of the potentially impor‑ and potential uses of this fascinating group of organ‑
tant role for interspecies interactions in bacterial viru‑ isms presents both considerable challenges and oppor‑
lence and the response to therapy. S. maltophilia can be tunities for the future. Determination of the genome
found together with the opportunistic pathogen P. aeru sequences of the clinical and endophytic S. maltophilia
ginosa in diverse niches, including the lungs of patients strains forms the basis for functional genomic analyses

REVIEWS
Riboswitch to test the contribution of specific functions to the infections or endophytic colonization, merits attention.
A conformational switch in tenacity of these bacteria in colonization, their broad Further insights into the role of Stenotrophomonas
RNA molecules that is induced resistance to antibiotics and their ability to enter into spp. in the nitrogen cycle should emerge from analy‑
by small metabolites and leads close endophytic associations with plants. These stud‑ sis of the genome of Stenotrophomonas sp. SKA14, a
to a switch in gene regulatory
function.
ies might also be expected to reveal alternative targets nitrogen‑fixing bacterium that was isolated from the
for antimicrobial action that could include interference Baltic Sea. The sequencing of other Stenotrophomonas
with quorum sensing or cell–cell signalling, interfer‑ spp., such as S. rhizophila, that have potential uses in
ence with the action of riboswitches and inhibition of promoting plant growth, biocontrol or bioremedia‑
adherence to surfaces and biofilm formation. Given tion but are not pathogenic are also warranted. Finally,
the ubiquitous nature of Stenotrophomonas spp., the Stenotrophomonas spp. should continue to be a source
impact of interactions with other organisms in pol‑ of useful or novel enzymatic capabilities, reflecting
ymicrobial communities, which may be associated with their metabolic versatility.
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REVIEWS

The versatility and adaptation

514 | july 2009 | VoluMe 7 www.nature.com/reviews/micro

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can produce extracellular enzymes (proteases, lipases,

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Pseudomonas trivialis DSM 14937T (AJ492831)

75/ Pseudoxanthomonas mexicana AMX 26BT (NR_025105)

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518 | july 2009 | VoluMe 7 www.nature.com/reviews/micro

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Box 1 | Stenotrophomonas species as a source of useful compounds and activities

Useful compound or activity refs

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© 2009 Macmillan Publishers Limited. All rights reserved

520 | july 2009 | VoluMe 7 www.nature.com/reviews/micro

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O antigen and Restriction and/or Phage and Glycosyl Chloramphenicol

NATuRe ReVIeWS | MicroBiology VoluMe 7 | july 2009 | 521

© 2009 Macmillan Publishers Limited. All rights reserved

Polymicrobial infections and interspecies signalling. Concluding remarks

522 | july 2009 | VoluMe 7 www.nature.com/reviews/micro

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NATuRe ReVIeWS | MicroBiology VoluMe 7 | july 2009 | 523

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