2009-2-Antibiotic Resistance Genes in Water Environment PDF

Appl Microbiol Biotechnol (2009) 82:397414
DOI 10.1007/s00253-008-1829-z
MINI-REVIEW
Antibiotic resistance genes in water environment

Xu-Xiang Zhang & Tong Zhang & Herbert H. P. Fang
Received: 25 October 2008 / Revised: 11 December 2008 / Accepted: 13 December 2008 / Published online: 8 January 2009
# Springer-Verlag 2008
Abstract The use of antibiotics may accelerate the development of antibiotic resistance genes (ARGs) and bacteria
which shade health risks to humans and animals. The
emerging of ARGs in the water environment is becoming
an increasing worldwide concern. Hundreds of various
ARGs encoding resistance to a broad range of antibiotics
have been found in microorganisms distributed not only in
hospital wastewaters and animal production wastewaters,
but also in sewage, wastewater treatment plants, surface
water, groundwater, and even in drinking water. This
review summarizes recently published information on the
types, distributions, and horizontal transfer of ARGs in
various aquatic environments, as well as the molecular
methods used to detect environmental ARGs, including
specific and multiplex PCR (polymerase chain reaction),
real-time PCR, DNA sequencing, and hybridization based
techniques.
Keywords Antibiotic resistance gene .
Environmental pollution . Gene transfer .
Molecular detection method . Water environment
X.-X. Zhang : T. Zhang (*) : H. H. P. Fang

Environmental Biotechnology Lab,
Department of Civil Engineering,
The University of Hong Kong,
Pokfulam Road,
Hong Kong, SAR, China
e-mail: zhangt@hkucc.hku.hk
X.-X. Zhang
Department of Environmental Science, Nanjing University,
Nanjing, China
Introduction
Antibiotics are widely used to protect the health of human
and animals or to increase growth rate of animals as food
additive. The majority of antibiotics are excreted unchanged into the environment. Thus, concerns about the
potential impact of antibiotic residues in the aquatic
environment keep growing in recent years (Sarmah et al.
2006; Wright 2007; Kemper 2008). In surface water, it is
difficult to find an area where antibiotics cannot be
detected, except for the pristine site in the mountains before
the rivers or streams going through urban or agricultural
areas (Yang and Carlson 2003). Some antibiotics can be
found even in groundwater as deep as more than 10 m (Batt
et al. 2006).
Apart from chemical pollution caused by antibiotics
themselves, the use of antibiotics may also accelerate the
development of antibiotic resistance genes (ARGs) and
bacteria, which shade health risks to humans and animals
(Kemper 2008). These bacteria might be transmitted from
environment to human via direct or indirect contact (Iversen
et al. 2004; Kim et al. 2005; Rodrguez et al. 2006).
Considering the growing evidences that clinical resistance
is intimately associated with environmental ARGs and
bacteria (Tatavarthy et al. 2006; Prabhu et al. 2007;
Abriouel et al. 2008), it is quite clear that the research
activities need to be expended to include nonpathogenic or
environmental microorganisms. Currently, there are a
number of publications relating to the occurrence of ARGs
in different water environments, but few reviews have been
done. This paper presents an overview of the latest
information available in the literature on the types,
distributions, and horizontal transfer of ARGs in various
aquatic environments, as well as the molecular methods
used to detect environmental ARGs.
398
Types of environmental ARGs

Applications of antibiotics in human, veterinary medicine, and
agriculture for nearly 60 years have exerted a major impact on
bacterial communities, resulting in various resistances to the
antibiotics, which is genetically controlled by ARGs. The use

of antibiotics results in hundreds of ARGs being detected in
various water environments (Tables 1, 2, 3, 4, and 5). These
environmental ARGs are mainly created by the following
mechanisms: (1) target bypass (dfrA1, A5, A7, A12, A15,
Table 1 Tetracycline resistance genes in water environments

Gene
Biological source
Tetracycline efflux protein

tetA
Aeromonas, Alcaligenes, Arthrobacter,
Comamonas, Escherichia, Listeria,
Pseudomonas, Salmonella, and Vibrio;
Plasmids pB10, pTB11 and pRSB101
tetA(41)
tetB
tetC
tetD
tetE
Serratia
Afipia, Alcaligenes, Arthrobacter,
Burkholderia, Escherichia,
Pseudomonas, Serratia,
Staphylococcus, and Vibrio
Aeromonas, Alcaligenes, Arthrobacter,
Brevibacterium, and Pseudomonas
Aeromonas, Escherichia;
microbial community
Aeromonas, Pseudoalteromonas, and Vibrio
tetG
tetH
Pseudomonas; microbial community

Aeromonas, Flavobacterium, Proteus,
Pseudomona, Staphylococcus, and Wautersiella
tetJ
Pseudomonas
tetY
Acidiovorax, Acinetobacter, Comamonas,
and Proteus
tetZ
Actinomycetales, Afipia, Brevibacterium,
Burkholderia, Dietzia, Leucobacter, and
Microbacterium
Alcaligenes, Arthrobacter, and Pseudomonas
tet33
tet39
Acinetobacter
otrB
Streptomycete
Ribosomal protection protein
tetB(P)
Microbial community
tetM
Aeromonas, Bacillus, Escherichia, Lactococcus,
Pseudoalteromonas, and Vibrio;
microbial community
tetO
Environmental sourcea
Reference
AS, DW, EW,

NW, SD, SW,
US
AS, DW, EW,

SW, US
AS, EW, SD,
SW, US
AS, EW, SW, US
SW
Szczepanowski et al. 2004; Agers and Sandvang

2005; Srinivasan et al. 2005; Tennstedt et al. 2005;
Poppe et al. 2006; Rodrguez et al. 2006; Cernat
et al. 2007; Dang et al. 2007; Macauley et al. 2007;
Hu et al. 2008
Thompson et al. 2007
Agers and Sandvang 2005; Cernat et al. 2007;
Dang et al. 2007; Jacobs and Chenia 2007;
Kim et al. 2007; Kobashi et al. 2007, Macauley
et al. 2007
Agers and Sandvang 2005; Akinbowale et al.
2007a; Macauley et al. 2007
Schmidt et al. 2001; Auerbach et al. 2007;
Cernat et al. 2007
Schmidt et al. 2001; Dang et al. 2006;
Agers and Petersen 2007
Auerbach et al. 2007; Macauley et al. 2007
Jacobs and Chenia 2007; Macauley et al. 2007
SW
SW
Macauley et al. 2007

Macauley et al. 2007
SW
Kobashi et al. 2007; Macauley et al. 2007
SW
SD, SW
AS, NW, SW
Agers and Sandvang 2005

Agers and Petersen 2007
Nikolakopoulou et al. 2005
SD, SW
AS, EW, NW, SD,
SW, US
Chee-Sanford et al. 2001; Pei et al. 2006

Mackie et al. 2006; Akinbowale et al. 2007b;
Auerbach et al. 2007; Dang et al. 2007;
Kim et al. 2007; Nonaka et al. 2007; Hu et al.
2008; Rahman et al. 2008; Suzuki et al. 2008
Chee-Sanford et al. 2001; Smith et al. 2004;
Mackie et al. 2006; Pei et al. 2006;
Auerbach et al. 2007; Nonaka et al. 2007
Smith et al. 2004; Auerbach et al. 2007;
Mackie et al. 2006
Chee-Sanford et al. 2001; Kim et al. 2004;
Auerbach et al. 2007; Suzuki et al. 2008
Chee-Sanford et al. 2001; Pei et al. 2006
Chee-Sanford et al. 2001; Mackie et al. 2006;
Pei et al. 2006; Suzuki et al. 2008
Chee-Sanford et al. 2001; Nikolakopoulou et al. 2005
NW
AS, DW, EW,
NW, SW, US
AS, EW, SW, US
tetQ
Paenibacillus, Pseudoalteromonas, Shewanella,

Sporosarcina, and Vibrio; microbial
community
Microbial community
tetS
Lactococcus and Vibrio; microbial community
tetT
tetW
Microbial community
Microbial community
AS, EW, NW,

SW, US
AS, EW, SD,
SW, US
SD, SW
SD, NW, SW
otrA
Streptomycete; microbial community
AS, NW, SW
AS, EW, NW, SD,

SW, US
The antibiotic resistance genes were detected in the following water environments: SW special wastewater from hospital, animal production, and
aquaculture area; US untreated sewage; AS activated sludge of sewage treatment plant; EW effluent water of sewage treatment plant; NW natural
water; SD sediments; and DW drinking water
399
Table 2 Aminoglycoside resistance genes in water environments

Gene
Biological source
Environmental Function
sourcea
Reference
aacA4
Plasmid pTB11
AS, NW
Aminoglycoside-6-Nacetyltransferase
aacA29b
aacC1
aacC2
Plasmid pTB11
Microbial communities
AS
NW, SW, US
NW, SW, US
Tennstedt et al. 2005; Mukherjee

and Chakraborty 2006
Tennstedt et al. 2003
Aminoglycoside-3-Nacetyltransferase
Lee et al. 1998; Heuer et al. 2002
aacC3
aacC4
aadA1
Aeromonas, Citrobacter and
Shigella; Plasmid pTB11
NW, SW, US
NW, SW, US
AS, EW, NW,
SW, US
aadA2
Aeromonas, Escherichia and Vibrio; AS, NW, SD,

Plasmids pB2, pB3 and pTB11
SW, US
aadA4
aadA5
aadA13
aadB
Plasmid pB8
Escherichia and Vibrio;
Plasmid pTB11
Aeromonas; Plasmid pTB11
Aeromonas
SW
AS
aphA1
Salmonella
DW, NW
aphA2
aphD
aph(3)-Ic
nptII
sat1
sat2
strA
Escherichia
Mycobacterium
Aeromonas and Escherichia
Aeromonas and Escherichia
Listeria, Salmonella and Vibrio;
Plasmids pB4 and pB10
DW
NW, SW, US
NW
NW, SW
NW, SW
AS, NW, SW
strB
Salmonella and Vibrio; Plasmids

pB4 and pB10
AS, NW
Aminoglycoside-3adenylyltransferase
AS
AS, NW
Aminoglycoside-2adenylyltransferase
Aminoglycoside
phosphoryltransferase
Tennstedt et al. 2003; Henriques et al.

2006a; Mukherjee and Chakraborty
2006; Moura et al. 2007
Dalsgaard et al. 2000; Tennstedt et al.
2003; Heuer et al. 2004;
Taviani et al. 2008
Schlter et al. 2005
Park et al. 2003; Tennstedt et al. 2003;
Mohapatra et al. 2008
Moura et al. 2007
Cernat et al. 2007; Poppe et al. 2006
Cernat et al. 2007

Heuer et al. 2002
Ramn-Garca et al. 2006
Neomycin phosphotransferase Zhu 2007
Streptothricin acetyltransferase Henriques et al. 2006a; Moura et al. 2007
Henriques et al. 2006a; Moura et al., 2007
Streptothricin
Tauch et al. 2003; Poppe et al. 2006;
phosphoryltransferase
Jacobs and Chenia 2007; Mohapatra
et al. 2008
Tauch et al. 2003; Poppe et al. 2006;
The abbreviations of environmental sources are the same as those in Table 1
A17, and 18; sulI, II, III, and A), inaccessibility of the
antibiotics to their target enzyme by mutational changes or
loss on the enzyme gene (Huovinen et al. 1995; Happi et al.
2005); (2) efflux pumps (cmlA1 and A5; floR; otrB; tetA,
A(41), B, C, D, E, G, H, J, Y, Z, 33 and 39), reduction of
intracellular concentrations of antibiotics by structural alteration of cellular membrane (Kumar and Schweizer 2005); (3)
antibiotic inactivation (aacC1, C2, C3, and C4; aadA1, A2,
A5, A13, and B; ampC; aphA1, D and (3)-Ic; blaOXA-1,
blaOXA-2, blaOXA-10, blaOXA-30, and blaPSE-1; mphA; nptII;
sat1 and 2; strA and B), direct deactivation of antibiotic
molecule (Wright 2005); or (4) target modification (ermA, B,
C, E, F, T, V, and X; mecA; penA; otrA; tetB(P), M, O, Q, S,
T, and W; vanA and B), modification of the action sites of
antibiotics (Lambert 2005). It is noteworthy that the
resistance of certain antibiotic may be associated with
different ARGs based on more than one mechanism.
ARGs related to tetracycline

Tetracycline-resistant bacteria were found to emerge in the
environments with the introduction of tetracycline (Dancer
et al. 1997). There have been at least 38 different
tetracycline resistance (tet) genes and three oxytetracycline
resistance (otr) genes characterized to date (Roberts 2005;
Thompson et al. 2007). These genes include 23 genes,
which code for efflux proteins (efflux pump mechanism),
11 genes for ribosomal protection proteins (target modification mechanism), and three genes for an inactivating
enzyme and one gene with unknown resistance mechanism
(Levy et al. 1999; Roberts 2005).
Among them, more than 22 tet or otr genes have been
found in bacterial isolates from water environments
(Table 1). Most environmental tet genes code for transport
proteins, which pump the antibiotics out of the bacteria
400
Table 3 Macrolide, chloramphenicol, and vancomycin resistance genes in water environments

Gene
Biological source
Macrolide resistance genes

ermA
Enterococcus
ermB
Bacillus and Enterococcus
ermC
Microbial community
ermE
Microbial community
ermF
Microbial community
ermT
Microbial community
ermV
Microbial community
ermX
Microbial community
mphA Plasmid pRSB101
Function
Reference
EW,
EW,
EW,
SW
EW,
EW,
SW
EW,
AS
Erythromycin resistance
methylase
Hayes et al. 2005; Chen et al. 2007

Hayes et al. 2005; Chen et al. 2007
Chen et al. 2007
Patterson et al. 2007
Chen et al. 2007
Chen et al. 2007
Patterson et al. 2007
Chen et al. 2007
Szczepanowski et al. 2004
SW
SW
SW
SW
SW
SW
Chloramphenicol resistance genes

cmlA1 Plasmid pB2 and pB3
cmlA5 Plasmid pTB11
catB2 Plasmid pTB11
catB3 Aeromonas
catI
Pseudomonas
catII
Vibrio
catIII
Pseudomonas
catIV
Vibrio and Pseudoalteromonas
Listeria, Pseudoalteromonas
floR
Salmonella and Vibrio,
Vancomycin resistance genes
vanA
Enterococcus and Staphylococci
DW, EW, NW, SW, UW
vanB
EW, NW, UW
Enterococcus
AS
AS
AS
SW
NW
SW
NW
SW
DW, NW, SW
Macrolide-2phosphotransferase
Chloramphenicol efflux
protein
Chloramphenicol
acetyltransferase
Florfenicol efflux
protein
Vancomycin resistance
protein
Heuer et al. 2004

Jacobs and Chenia 2007
Dang et al. 2008
Dang et al. 2007
Dang et al. 2008
Dang et al. 2006
Srinivasan et al. 2005; Poppe et al. 2006;
Dang et al. 2007
Schwartz et al. 2003; Volkmann et al. 2004;
Messi et al. 2006
Iversen et al. 2002; Caplin et al. 2008
cell and keep the intercellular concentrations low to make

ribosomes function normally (Roberts 2002). The efflux
genes of tetA, B, C, D, and E frequently appeared in
various environmental compartments including activated
sludge of sewage treatment plants (STPs) (Guillaume et al.
2000), fish farming ponds (Schmidt et al. 2001; Dang et
al. 2007), surface water (Poppe et al. 2006), and swine
lagoon (Macauley et al. 2007). Recently, the tetracycline
resistance genes including tetM, O, S, Q, and W, coding
for ribosomal protection proteins, have also been detected
in microbial communities of sewage treatment systems
(Auerbach et al. 2007), hospital or animal production
wastewaters (Kim et al. 2007; Nonaka et al. 2007), and
even in natural water environments (Mackie et al. 2006).
Many tet genes are located on nonmobile plasmids or
incomplete transposons in the chromosome (Roberts 2005),
but some genes encoding efflux enzymes (tetA, B, C, E, H,
Y, Z, and 33) and ribosomal protection proteins (tetM and O)
still have a broad host range and have been found in several
environmental genera including Gram-negative and Grampositive species (Table 1). Recently, Agers and Petersen
(2007) have found that tetE is often located on large
horizontally transferable plasmids of Aeromonas spp. isolated from pond water of fish farm, and the gene has been
proved to be capable of interspecies transfer to Escherichia

coli. tetA, D, and M can also be transferred horizontally by
oxytetracycline resistance plasmid from environmental
microorganisms to E. coli strains isolated from chicken,
pig, and human, which indicates the potential environmental
hazards caused by the tet ARGs (Akinbowale et al. 2007b).
ARGs related to aminoglycoside
Different from tetracycline resistance mechanisms mentioned above, the most major mechanism of aminoglycoside resistance is direct deactivation of this type of
antibiotics by enzymatic modification (Shakil et al. 2008).
More than 50 modification enzymes have been found so far
(Vakulenko and Mobashery 2003; Ramn-Garca et al.
2006). These enzymes are divided into three groups based
upon their biochemical actions on the aminoglycoside
substrates, including acetyltransferases, phosphotransferases, and nucleotidyltransferases (adenylyltransferases),
encoded by three types of genes, namely, aac, aph, and ant
(aad), respectively. Different aminoglycoside-modifying
enzymes have been reported in a broad range of bacteria
isolated from patients or clinical environments (Filipova
et al. 2006; Kelmani Chandrakanth et al. 2008).
401
Table 4 Sulphonamide and trimethoprim resistance genes in water environments

Gene
Biological source
Dihydrofolate reductase encoding genes

dfrA1
Aeromonas, Escherichia, and Salmonella
dfrA5
Escherichia
dfrA7
Escherichia
dfrA12 Aeromonas, Escherichia, and Salmonella
dfrA15 Vibrio
dfrA17 Escherichia, Salmonella
dfr18
Vibrio
Dihydropteroate synthase encoding genes
sulI
Aeromonas, Escherichia, and Listeria;
Plasmids pB2, pB3, pB8, and pB10;
Microbial community
sulII
Acinetobacter, Escherichia, Salmonella,
and Vibrio; Microbial community
sulIII
Escherichia; Microbial community
sulA
Microbial community
a
Reference
NW, SW
Henriques et al. 2006a; Mukherjee and Chakraborty 2006;

Moura et al. 2007
Park et al. 2003; Mukherjee and Chakraborty 2006
Park et al. 2003
Moura et al. 2007; Antunes et al. 2006; Cernat et al. 2007
Park et al. 2003; Taviani et al. 2008
Park et al. 2003; Antunes et al. 2006; Cernat et al. 2007
NW
NW
DW, NW, SW
EW, NW
DW, NW
NW
AS, DW, NW, SD, SW
DW, NW, SD, SW

NW, SD
SD
Heuer et al. 2004; Lin and Biyela 2005; Schlter et al. 2005;
Srinivasan et al. 2005; Akinbowale et al. 2007a;
Cernat et al. 2007; Hu et al. 2008
Pei et al. 2006; Agers and Petersen 2007; Cernat et al. 2007;
Hu et al. 2008; Mohapatra et al. 2008;
Pei et al. 2006; Hu et al. 2008
Pei et al. 2006
The abbreviations of environmental sources are the same as those in Table 1.
The aac, aph, and ant genes are widely distributed in

various genera including Aeromonas, Escherichia, Vibrio,
Salmonella, and Listeria spp. isolated from polluted or
natural water environments (Table 2). The genes of aacC1,
C2, C3, and C4, encoding aminoglycoside-3-N-acetyltransferase, were often detected in microbial communities or
isolates from STPs (Heuer et al. 2002; Tennstedt et al.
2003, 2005), and the two adenylyltransferase genes, aadA1
and aadA2, were frequently reported all around the world
in the isolates from aquaculture areas (Dalsgaard et al.
2000), river water (Park et al. 2003), STPs (Szczepanowski
et al. 2004; da Silva et al. 2007), and surface urban water
(Taviani et al. 2008).
ARGs encoding resistances to other antibiotics in aminoglycoside group, for example, phosphotransferase genes
encoding resistance to neomycin (nptII) and streptothricin
(strAB), have also been detected in the river water of
Canada (Zhu 2007) and Ganges river of India (Mohapatra
et al. 2008).
ARGs related to macrolidelincosamidestreptogramin,
chloramphenicol, and vancomycin
Although structurally unrelated to each other, the three
antibiotics, macrolides, lincosamide, and streptogramin, are
often investigated simultaneously for microbial resistance,
since some macrolide resistance genes (erm) encode
resistance to two or all three of these compounds (Roberts
et al. 1999). Totally, more than 60 different genes confer
resistance to one or more of the macrolidelincosamide
streptogramin (MLS) antibiotics have been identified
(Roberts 2008), including the genes associated with
ribosomal RNA (rRNA) methylation, efflux, and inactivation. MLS resistance is mostly mediated by rRNA
methylases (encoded by erm genes), which methylate the
adenine residues to prevent the three antimicrobials from
binding to ribosomal protein (Roberts 2002; Cetin et al.
2008). The erm genes can easily be transferred from one
host to another (Roberts 2003), since they are usually
acquired and associated with mobile elements, such as
plasmids (Liu et al. 2007) and transposons (Okitsu et al.
2005).
Several erm genes have been detected in Enterococcus
spp. isolated from poultry raising wastewaters (Hayes et al.
2005) and environmental DNA extracted from livestock
manures (Chen et al. 2007; Table 3). Six classes of erm
genes (A, B, C, F, T, and X) have been detected and
quantified in the samples from animal production matures,
lagoons, and a biofilter system treating hog house effluents
(Chen et al. 2007). Among the macrolide resistance
determinants, ermB is considered as the most prevalent gene
in environmental microorganisms, especially in the strains of
Enterococcus (Hayes et al. 2005) and Streptococcus spp.
(Jensen et al. 2002).
The mechanisms responsible for resistances to chloramphenicol and florfenicol include chloramphenicol acetyltransferases (encoded by cat genes), specific exporters (encoded
by cml genes), and multidrug transporters (Schwarz et al.
2004). Of the chloramphenicol resistance genes known to
date, several types of cat or cml genes have been reported to
be of environmental origin (Table 3). Vancomycin resistance
firstly emerged in enterococci, and recently, the resistance
has also been detected in Staphylococcus aureus (Walsh and
Howe 2002). So far, six types of vancomycin resistance
402
Table 5 -Lactam and penicillin resistance genes in water environments

Gene
Biological source
Environmental sourcea Function
ampC
Enterobacter, Salmonella
DW, NW, SW, US
blaPSE-1
Aeromonas, Salmonella and Vibrio EW, SD, SW, US
blaTEM-1
blaOXA-1
blaOXA-2
Escherichia
Plasmid pTB11
Aeromonas; Plasmids pB8,
pB10 and pTB11
Plasmid pTB11
DW
AS
AS, EW, SW
AS
Schwartz et al. 2003; Volkmann et al. 2004;

Poppe et al. 2006
Dalsgaard et al. 2000; Jacobs and Chenia 2007;
Taviani et al. 2008
TEM-type -lactamase Alpay-Karaoglu et al. 2007; Cernat et al. 2007
OXA-1 -lactamase
OXA-2 -lactamase
Schlter et al. 2005; Tennstedt et al. 2005;
Jacobs and Chenia 2007
OXA-10 -lactamase Tennstedt et al. 2003
Salmonella
SW
OXA-30 -lactamase
Antunes et al. 2006; Moura et al. 2007
mecA
Staphylococcus
DW, NW, US
Penicillin-binding
protein
Schwartz et al. 2003; Volkmann et al. 2004
penA
Listeria
DW, SW
blaOXA-
Reference
AmpC type
-lactamase
PSE-1-lactamase
10
blaOXA30
Srinivasan et al. 2005
genes (van) have been known (Messi et al. 2006), and vanA
and vanB are the most prevalent ones in water environments
(Table 3).
ARGs related to sulfonamides and trimethoprim
Sulfonamides are the first antibiotic developed for largescale introduction into clinical use, which target dihydropteroate synthase (DHPS). Trimethoprim competitively
inhibits dihydrofolate reductase (DHFR), which is responsible for the reduction of dihydrofolate to tetrahydrofolate
(Alekshun and Levy 2007). The two types of bio-enzymes
are partly responsible for folate bio-synthesis, which is
associated with thymine production and microbial growth
(Nrochet et al. 2008). Resistances to sulfonamides and
trimethoprim are often encoded by mutations located on
highly conserved areas of DHPS genes (sul) and DHFR
genes (dfr) (Skld 2000, 2001). Different types of mechanisms have been found to confer to sulfonamide resistance,
mostly based on changes in the sul genes and mediation by
mobile elements (Huovinen et al. 1995; Antunes et al. 2007).
The most widespread trimethoprim resistance mechanism is
the replacement of a trimethoprim-sensitive DHFR by a
plasmid-, transposon-, or cassette-borne trimethoprim-resistant DHFR (Skld 2001; Blahna et al. 2006).
Four kinds of sul genes (sulI, II, III, and A) have been
found in the bacteria of environmental origin (Table 4). sulI
and II have been detected in bacterial isolates from fecal
slurry of dairy farms (Srinivasan et al. 2005), water or
sediments of aquaculture areas (Akinbowale et al. 2007a;
Agers and Petersen 2007), and even from the river or sea
water without evidence of being polluted (Lin and Biyela
2005; Hu et al. 2008; Mohapatra et al. 2008). sulI, as a part
of class 1 integron, can be disseminated and transferred

horizontally within and between bacterial species in
wastewater (Tennstedt et al. 2003), river water (Mukherjee
and Chakraborty 2006), and sea water (Taviani et al. 2008).
More than 25 different resistant DHFR genes (dfr),
subdivided into dfrA and dfrB, have been identified
(Kehrenberg and Schwa 2005; Didi et al. 2008), and
several dfrA genes are commonly found in various
environmental isolates (Table 4). The environmental
habitats of these genes include urban wastewater treatment
plants (da Silva et al. 2007), slaughterhouse wastewater
treatment plants (Moura et al. 2007), aquaculture systems
(Jacobs and Chenia 2007), and river water (Park et al.
2003; Mukherjee and Chakraborty 2006; Mohapatra et al.
2008). dfrA1 is one of the static resistance genes located
on class 2 integrons (Blahna et al. 2006), and dfr gene
cassettes are frequently found in the variable regions of
integrons and are often the only gene cassettes present in
environmental isolates (Antunes et al. 2006; Mukherjee
and Chakraborty 2006).
ARGs related to -lactam
-Lactams are the most widely used antibiotics, and resistance
to these antibiotics is a severe threat because they have low
toxicity and are used to treat a broad range of infections
(Livermore 1996). The mechanisms of -lactam resistance
include inaccessibility of the antibiotics to their target
enzymes, modifications of target enzymes, and/or direct
deactivation of the antibiotics by -lactamases (Walsh 2000;
Li et al. 2007). In Gram-negative bacteria, the primary
resistance mechanism is enzymatic inactivation through the
cleavage of the -lactam ring by -lactamases. More than 400
different -lactamases encoded by hundreds of ARGs (bla)

have been identified, and the enzymes are divided into four
molecular classes, AD, mediating resistances to a broad
range of -lactams including penicillins and cephalosporins
(Li et al. 2007).
A variety of bla genes (Table 5) have been identified in
bacteria derived from fecal slurry and lagoon water of dairy
farms (Srinivasan et al. 2005), water or sediments of
aquaculture areas (Dalsgaard et al. 2000; Jacobs and Chenia
2007), STPs (Szczepanowski et al. 2004; Volkmann et al.
2004; Antunes et al. 2006; Taviani et al. 2008), and surface
water (Schwartz et al. 2003; Poppe et al. 2006). The
environmental compartments may further serve as reservoirs for -lactam resistance genes. The bla genes are often
detected in animal-derived environmental pathogens including Aeromonas (Tennstedt et al. 2005; Jacobs and
Chenia 2007), Enterobacter (Volkmann et al. 2004),
Salmonella (Antunes et al. 2006; Moura et al. 2007),
Staphylococcus (Schwartz et al. 2003; Volkmann et al.
2004), and Vibrio spp. (Dalsgaard et al. 2000; Taviani et al.
2008). ampC gene encoding -lactamases has been
detected in the microbial isolates from wastewater, surface
water, and even from drinking water films (Schwartz et al.
2003). mecA gene encoding methicillin resistance in
staphylocci was observed to be prevalent in hospital
wastewater biofilms (Schwartz et al. 2003).
bla genes often coexist with other antimicrobial
resistance determinants and can also be associated with
mobile genetic elements, increasing the possibility of
multidrug resistance and environmental dissemination
(Tennstedt et al. 2003; Weldhagen 2004; Schlter et al.
2007b). The plasmids containing bla obtained from a
wastewater treatment plant are frequently associated with
transposons and integrons and often simultaneously carry
other resistance determinants including aad (or aac)
encoding aminoglycoside nucleotidyltransferase (or acetyltransferase), cml encoding chloramphenicol efflux
protein, and cat encoding chloramphenicol acetyltransferase (Tennstedt et al. 2003).
Molecular techniques for the detection

and characterization of environmental ARGs
Considering that ARGs are widespread in aquatic environments mentioned above, there is a need for the development
and application of molecular methods to investigate the
occurrence, transport, and fate of the environmental ARGs.
So far, the methods used for detection, typing, and
characterization of ARGs have covered, but not been
limited to, specific and multiplex polymerase chain reaction
(PCR), real-time PCR, DNA sequencing, and hybridization-based techniques including microarray.
403
DNA hybridization
Molecular hybridization has been used to detect presence/
absence of specific ARGs for nearly 30 years (Mendez
et al. 1980). Many improvements have been made on
molecular hybridization, especially in probe design and
synthesis, so that the technique, especially Southern blot, is
still often applied to distinguish different ARGs in one
group (i.e., tet genes) from each other (Roberts and Kenny
1986; Levy et al. 1999) or to identify presence of specific
genes in certain environment (Agers and Petersen 2007;
Malik et al. 2008). Southern hybridization and filter-mating
experiments demonstrated that tet and class 1 integrons can
be co-transferred from soil isolates to E. coli and/or
Pseudomonas putida (Agers and Sandvang 2005). Using
Southern blot or dot blot coupled with PCR method, Malik
et al. (2008) found that ampC was frequently present in soil
samples irrigated with wastewater. PCR-Southern blot
assays showed that tet39 and sulII were common resistance
genes in Acinetobacter spp. isolates from water and
sediments of fish farms.
With a number of nonradiolabeled systems becoming
commercially available, radioactive labeling is no longer an
option to label probes. As an important nonradiolabeled
method, fluorescence in situ hybridization (FISH) has been
established and implemented successfully for clinical
detection of microbial resistances. The use of FISH
technique has been described for the rapid identification
of macrolide resistances caused by ribosomal mutations
(Russmann et al. 2001). Recently, Werner et al. (2007) has
performed a research to evaluate the reliability of FISH for
clinical detection of linezolid-resistant enterococci and
found that the FISH technique along with DNA probes
containing locked nucleic acids with point mutation showed
100% sensitivity for the detection of phenotypic linezolid
resistance and even allowed detection of a single mutated
23S rRNA gene allele in phenotypically linezolid-susceptible enterococci. Moosavian et al. (2007) developed and
validated the FISH method for rapid detection of clarithromycin-resistant Helicobacter pylori in patients. Although
FISH has been often used for clinical detection of antibiotic
resistance, so far, few reports have been found about its use
in identification of target bacteria harboring ARGs in
environmental samples.
PCR (simple and multiplex PCR)
PCR assays have been widely used in both pure cultures
and mixed environmental samples for detection of specific
ARGs encoding resistances to aminoglycoside (Mohapatra
et al. 2008; Taviani et al. 2008), chloramphenicol (Dang
et al. 2008), -lactam (Taviani et al. 2008), macrolide
(Chen et al. 2007; Patterson et al. 2007), penicillin
404
(Srinivasan et al. 2005), sulphonamide (Agers and

Petersen 2007), tetracycline (Jacobs and Chenia 2007),
trimethoprim (Moura et al. 2007), and vancomycin (Caplin
et al. 2008). Environmental target DNA or RNA at low
concentrations can be amplified and detected by PCR-based
methods. However, a false-positive result is often given in the
PCR assay. Southern hybridization of PCR products labeled
and used as DNA probes to plasmid or chromosome DNA
samples from strains harboring target genes can avoid the
false-positive PCR results (Ahmed et al. 2006; Akinbowale
et al. 2007b). In addition to DNA hybridization, DNA
sequencing is another common method used to verify the
PCR products of certain ARGs (Thompson et al. 2007).
In order to save time and effort, multiplex PCR methods
have been developed and often used for simultaneous
detection of more than one environmental ARG, including
the genes encoding resistances to vancomycin (Bell et al.
1998), macrolide (Jensen et al. 2002), tetracycline (Ardic et
al. 2005; Agers et al. 2007), sulfamethoxazole, and
trimethoprim (Ramachandran et al. 2007). With various
primer pairs in the same PCR reaction system, multiplex
PCR can amplify the DNA fragments of several ARGs at
the same time (Gilbride et al. 2006). The method saves
considerable time and cost when different target regions are
investigated simultaneously, but as a result of all the
reactions taking place at the same conditions, some DNA
amplifications can be inhibited and false-negative results
are probably obtained. Another disadvantage of multiple
PCR is that the dimer formation between primer pairs can
disturb experimental results and lead to poor sensitivity
(Markoulatos et al. 2002). Despite of the drawbacks
mentioned above, multiplex PCR is still considered as a
rapid and convenient method for the detection of multiple
ARGs in isolated bacteria or environmental DNA (Agers
et al. 2007; Gilbride et al. 2006).
Quantitative PCR
The quantitative real-time PCR (qRT-PCR) is usually used to
quantify target DNA on the basis of the principle that initial
concentration can be estimated according to the change of
PCR product concentration with amplification cycles (Zhang
and Fang 2006). Among the several fluorescent reagents
developed for qRT-PCR, SYBR Green is the most common
method used to quantify ARGs in bacterial isolates of
clinical origin, including tet (Morsczeck et al. 2004), mef,
and erm genes (Reinert et al. 2004). Recently, the technique
has been frequently used to quantify ARGs in environmental samples, including tet genes in beef cattle farms (Yu et
al. 2005), groundwater (Mackie et al. 2006), river sediments (Pei et al. 2006), and STPs (Auerbach et al. 2007), as
well as sul genes in river sediments (Pei et al. 2006) and npt
genes in river water (Zhu 2007).
TaqMan probe, another fluorescent reagent, has also

been used to quantify tetO, tetW, and tetQ (Smith et al.
2004), as well as vanA, mecA, and ampC genes (Volkmann
et al. 2004) in wastewater. Chen et al. (2007) validated
TaqMan method for quantifying erm genes conferring
resistance to MLS in the environmental samples from
animal production areas.
The qRT-PCR method is not only usually used for
quantitative analysis on ARGs distribution in the environments but is also often applied to study the effects of
environmental factors or treatment processes on removal of
some ARGs, i.e., tet genes (Mackie et al. 2006; Auerbach
et al. 2007), sul genes (Pei et al. 2006), and erm genes (Chen
et al. 2007). Using qRT-PCR, Auerbach et al. (2007)
investigated tet genes in Germany STPs and found that tetQ
concentrations were highest in influent water while tetG
concentrations were highest in activated sludge, and UV
disinfection had no effects on reduction in the amount of
detectable tet genes in wastewater effluent. In order to
analyze the effect of river landscape on distributions of
ARGs in sediments, some tet and sul genes in the sediments
have been quantified using qRT-PCR, and higher resistance
gene concentrations have been obtained at the impacted sites
than at the pristine site (Pei et al. 2006). Using real-time
PCR, Mackie et al. (2006) found that detection frequency of
tetM, O, Q, and W genes was much higher in wells located
closer to and down-gradient from swine lagoons than in wells
more distant from the lagoons. With qRT-PCR, Chen et al.
(2007) found that erm abundances in composted swine
manure samples were significantly lower than those in swine
manure, demonstrating that manure storage probably influences the persistence of the environmental genes.
DNA Microarray
Compared with other molecular methods, DNA microarray
technique is a genomic analysis technique with highthroughput, high-speed and high-delicacy. For detection of
antibiotic resistances, DNA microarray can provide detailed,
clinically relevant information on the isolates by detecting
the presence or absence of a large number of ARGs
simultaneously in a single assay (Gilbride et al. 2006).
Microarray allows detection of antibiotic resistance determinants within several hours and can be used as a time-saving
and convenient tool supporting conventional resistance
detection assays (Antwerpen et al. 2007). Microarray has
been widely used to clinically detect antibiotic resistance of
human pathogens E. coli (Zhu et al. 2007a), H. pylori (Chen
et al. 2008a), Salmonella enterica (Guard-Bouldin et al.
2007), and S. aureus (Zhu et al. 2007b; Spence et al. 2008).
The technique can also be applied to analyze genotypic
resistance mechanisms of certain antibiotics (Chen et al.
2008b).
Although microarrays have been successfully used to

assess the antibiotic resistances of clinical samples, few
reports are found about using this technique to detect the
ARGs in environmental samples. The first factor hampering
its application in environmental samples is the low
detection limit of the method, but microarray coupled with
PCR method can enhance the detection limit for environmental ARGs (Gilbride et al. 2006). Patterson et al. (2007)
developed a microarray system based on PCR amplification
of 23 tet genes and 10 erm genes to screen environmental
samples for the presence of these ARGs and found that
tetW, O, and Q were the most abundant ARGs found in
swine fecal samples and ermV, and E were the most
common ones detected in farm and garden soil samples.
Another reason for the poor applications of microarray in
most environmental samples is the complexity of the
samples and pretreatment. The presence of undesirable
contaminants in environmental samples inhibits DNA
extraction and/or target gene amplification, so the complicated pretreatment of environmental samples is necessary
and crucial to get satisfactory detection results (Call 2005).
Microarray technique can provide a detailed description of
bacterial antibiotic resistance and can reveal global changes
in ARG expression in response to environmental changes
(Call et al. 2003; Gilbride et al. 2006). The information on
gene expression provides insight into antibiotic resistance
mechanisms and general genetic responses of ARGs to
environment-related changes.
Geographical distribution of studying ARGs in water

environment
The geographical distribution of environmental ARGs has
been indicated in the studies and detections on the genes
all around the world (Fig. 1). In Europe, nearly all types
of ARGs were frequently detected in aquatic environments
of some countries, including Germany (Tennstedt et al.
2003; Szczepanowski et al. 2004; Tennstedt et al. 2005;
Nikolakopoulou et al. 2005), Portugal (Antunes et al.
2006; da Silva et al. 2007; Moura et al. 2007), Belgium
(Guillaume et al. 2000; Heuer et al. 2002; Nikolakopoulou
et al. 2005), Denmark (Schmidt et al. 2001; Agers and
Sandvang 2005), and Greece (Heuer et al. 2002). Various
water bodies in Europe have been found to contain some
common ARGs, for example, vancomycin resistance
genes van, which have been detected in dairy farm water
of Italy (Messi et al. 2006), human-derived wastewater of
England (Caplin et al. 2008), urban raw sewage, treated
sewage and surface water of Sweden (Iversen et al. 2002),
municipal wastewater, surface water, and drinking water
biofilms of Germany (Schwartz et al. 2003; Volkmann
et al. 2004).
405
In Northern America, tetracycline resistance genes were

frequently detected in water environments, including lagoon
water (Chee-Sanford et al. 2001; Srinivasan et al. 2005;
Macauley et al. 2007), surface water (Poppe et al. 2006;
Thompson et al. 2007), and wastewater treatment systems
(Mispagel and Gray 2005; Auerbach et al. 2007). Other
environmental ARGs have also been found in the continent,
encoding a wide resistance to aminoglycoside (Zhu 2007),
-lactam (Srinivasan et al. 2005), chloramphenicol (Poppe
et al. 2006), macrolide (Chen et al. 2007), and sulfonamide
(Pei et al. 2006). However, environmental distribution of
ARGs has seldom been reported in Southern America.
In Asia, about 10 years ago, researchers began
investigating ARGs distribution in aquatic environments
(Lee et al. 1998). dfr (Park et al. 2003) and tet genes
(Suzuki et al. 2008) were detected in water samples of
Asian rivers, and tet genes were also found in marine
aquatic environments in Korea (Kim et al. 2004; Kim et al.
2007) and Japan (Nonaka et al. 2007; Rahman et al.
2008). In China, chloramphenicol (catI, II, III, and IV)
and tetracycline resistance genes (tetA, B, D, E, and M)
have been detected in aquaculture ponds (Dang et al.
2006; Dang et al. 2007) and coastal marine water (Dang et
al. 2008). Recently, several tet and sul genes have also
been found in natural river basin of China (Hu et al.
2008). In India, ARGs occurring in river water confer
resistances to aminoglycoside, sulfonamide, and trimethoprim (Mukherjee and Chakraborty 2006; Mohapatra et al.
2008). In Thailand, ARGs related to aminoglycoside and
lactam resistances (Dalsgaard et al. 2000), as well as
sulfonamide and tetracycline resistances (Agers and
Petersen 2007) were detected in the sediments of fish or
shrimp production areas.
Investigations about environmental ARGs have also been
carried out in Africa and Australia. Akinbowale et al.
(2007a) found that Aeromonas containing resistance genes
and class 1 integrons were present in sediments of fish
farms of Australia. Plasmids and integrons carrying a
variety of ARGs have been identified in bacteria isolated
from South African aquaculture systems in the absence of
antibiotic selection pressure (Jacobs and Chenia 2007).
Class 1 integrons and integrating conjugative elements
conferring resistances to trimethoprim, aminoglycoside, and
-lactam were found in Vibrio strains isolated from surface
urban water in Mozambique (Taviani et al. 2008).
Habitates of ARGs in water environment

ARGs are prevalent in different water bodies, and the
spread pathways of ARGs in various aquatic environments
usually are complicated. Before learning about the fate and
transport of ARGs in the environments, it is necessary to
406
Fig. 1 Detection of the antibiotic resistance genes in geographically isolated water

environments, including the
genes encoding resistance to
aminoglycoside (red square),
chloramphenicol (brown
inverted triangle), -lactam
(plus symbol), macrolide (sky
blue triangle), sulfonamide (violet diamond), tetracycline
(green circle) and trimethoprim
(indigo star)
characterize the occurrence, and the first step in this

endeavor is to identify major habitats of the ARGs in the
environments. As a result of extensive use of human and
veterinary antibiotics, hospital wastewater and livestock
manure are considered as the major sources of environmental ARGs. ARGs can enter into aquatic environments
by direct discharging of untreated wastewater or into STPs
through wastewater collection systems and subsequently
into the environments with effluents and discharged sludge
(Auerbach et al. 2007). ARGs can be transferred into soils
by amending farm land with animal manure and processed
biosludge from STPs and then can leach to groundwater or
be carried by runoff and erosion to surface water (Yang and
Carlson 2003). Surface water and shallow groundwater are
commonly used as source of drinking water; thus, ARGs
can go though drinking water treatment facilities and enter
into water distribution systems (Schwartz et al. 2003).
Special wastewater from hospital, animal production,
and aquaculture areas
The broad use of human, veterinary, and aquaculture
antibiotics may exert selective pressure on bacteria in the
environments of hospital (Liu et al. 2007), animal production (Agers and Sandvang 2005), and fishery areas
(Agers and Petersen 2007), which are thought to be main
sources of ARGs distributing into the environments.
Among all classes of ARGs, tet genes have the highest
detection frequency, and about 20 types of tet genes have
been found in these wastewaters around the world,
including tetA (Srinivasan et al. 2005), tetB (Dang et al.
2007), tetC (Akinbowale et al. 2007a), tetD, and tetE
(Schmidt et al. 2001), tetG, J, Y, and Z (Macauley et al.
2007), tetH (Jacobs and Chenia 2007), tetM (Akinbowale
et al. 2007b), tetO (Nonaka et al. 2007), tetQ (Smith et al.
2004), tetW (Mackie et al. 2006), tetS (Kim et al. 2004),

tetB(P) and T (Chee-Sanford et al. 2001), tet33 (Agers and
Sandvang 2005), tet39 (Agers and Petersen 2007), and
otrA and B (Nikolakopoulou et al. 2005).
Other ARGs frequently detected in these special
wastewaters include methicillin resistance gene (mecA)
in staphylococci isolated from hospital wastewater biofilms (Schwartz et al. 2003), chloramphenicol resistance
genes (catII, IV and B3) in the aquaculture systems (Dang
et al. 2006; Dang et al. 2007; Jacobs and Chenia 2007),
and sulfonamide resistance genes (sulI, II, III, and A) in
fish farms (Agers and Petersen 2007). Additionally, some
types of ARGs including floR, penA, and strA (Srinivasan
et al. 2005), as well as bla genes (Henriques et al. 2006b),
were reported to occur in fecal slurry or lagoon of animal
production areas. ARGs in these wastewaters are directly
exposed to the environment and can eventually be transported to the nearby streams, rivers, lakes, or other
aquatic bodies or leach downward through the soil during
rainfall.
Untreated sewage
During the recent several years, various bacteria species
isolated from untreated sewage were found to contain a
variety of ARGs encoding resistances to aminoglycoside
(da Silva et al. 2007; Taviani et al. 2008), -lactam
(Schwartz et al. 2003; Volkmann et al. 2004; Antunes et
al. 2006), trimethoprim (da Silva et al. 2007), tetracyclines
(Auerbach et al. 2007), and vancomycin (Iversen et al.
2002; Caplin et al. 2008). By direct PCR of ARGs in
environmental DNA extracted from municipal wastewater,
tet genes (Auerbach et al. 2007) and aminoglycoside
resistance genes (aacC1, C2, C3, C4, aadB, and aphD)
(Heuer et al. 2002) were also found in sewage wastewaters.
Sewage receives the bacteria previously exposed to

antibiotics from private households and hospitals and is
considered as a hotspot for ARGs. ARGs go into STPs
with sewage water, and most of them cannot be
effectively removed with traditional treatment process
before being released into the environments (Volkmann
et al. 2004; Auerbach et al. 2007). Moreover, environmental conditions of activated sludge or biofilms facilitate
horizontal transfer of the ARGs from one host to another
because of the nutritional richness and high bacterial
density and diversity (Tennstedt et al. 2003; Schlter et al.
2007b).
STP activated sludge or biofilms
Several previous studies have shown that STPs serve as
important reservoirs for various ARGs (Smalla and
Sobecky 2002; Tennstedt et al. 2003; Schlter et al.
2007b). ARGs present in STPs encode a broad resistance
to antibiotics including aminoglycoside (Tennstedt et al.
2005; Moura et al. 2007), tetracycline (Guillaume et al.
2000; Mispagel and Gray 2005; Auerbach et al. 2007),
quinolone (Bnemann et al. 2006), and -lactam (Szczepanowski et al. 2004; Taviani et al. 2008). STPs receive
the antibiotic-resistant bacteria with the inflow sewage
water originating from hospitals, private households,
industry, and agriculture, so they play important roles in
recombination, exchange, and spread of environmental
ARGs (Szczepanowski et al. 2004).
STPs are recognized as important interfaces between
different water bodies, such as hospital wastewater,
domestic wastewater, surface water, and groundwater,
therefore may facilitate gene exchange and spread between
these environmental compartments (Schlter et al. 2007b).
Firstly, the presence of antibiotics in sewage selects for the
maintenance of ARGs conferring resistance in activated
sludge (Kmmerer 2003). Secondly, high microbial
density and diversity of biofilms and activated sludge
may facilitate genetic exchange in sewage treatment
bioreactors (Schlter et al. 2007b); for example, some tet
genes preferentially migrate from wastewater to biofilm
(Engemann et al. 2008). Additionally, various mobile
elements at high density in STPs accelerate gene recombination and transfer that encode new or multiple
antimicrobial resistances (Tennstedt et al. 2003; Schlter
et al. 2007a). Finally, many ARGs, for example, vanA and
B, cannot be effectively removed by activated sludge
process widely used in STPs, the genes being found in
both influent and effluent water (Iversen et al. 2002;
Caplin et al. 2008). ARGs enter into other water bodies
with effluent water and can be transferred horizontally to
the native bacteria in these aquatic environments
(Schwartz et al. 2003).
407
STP effluent water

STP effluent and sludge application to agricultural fields
are recognized as important sources of ARGs to surface
waters and soils and subsequently into groundwater (Yang
and Carlson 2003). Several reports have indicated that
bacteria harboring ARGs can be released from STPs into
surface waters (Tennstedt et al. 2005; Chen et al. 2007;
Auerbach et al. 2007).
Some types of ARGs have been detected in STP
effluent water including van genes (Iversen et al. 2002),
aac, aad, and oxa genes (Tennstedt et al. 2005), tet genes
(Auerbach et al. 2007), erm genes (Chen et al. 2007), and
bla and dfr genes (Taviani et al. 2008). Some aminoglycoside and -lactam resistance determinants in effluent water
are recombined into integrons horizontally transferred by
plasmids or transposons (Tennstedt et al. 2005). Resistance
determinants in bacteria have been detected from habitats
downstream of STPs (da Silva et al. 2007; Taviani et al.
2008), and antibiotic resistance regions can be extended,
modified, recombined, and exchanged in and among
bacteria residing in these areas (Schlter et al. 2007b).
New resistance properties could be horizontally transferred
to human pathogens, thus increasing the difficulties of
infectious disease treatment and threatening public health
(Iversen et al. 2004).
Natural water
Scores of ARGs have been found in the isolates or
microbial communities in the natural waters, which were
not or slightly polluted (Jacobs and Chenia 2007; Mohapatra
et al. 2008; Rahman et al. 2008). Several types of
aminoglycoside resistance genes have been detected in the
microorganisms isolated from surface water, including aac
(Lee et al. 1998), aad (Park et al. 2003; Mukherjee and
Chakraborty 2006), aph (Poppe et al. 2006), npt (Zhu
2007), and str (Mohapatra et al. 2008). The detection
frequency is also high for sulfonamides resistance genes (sul)
(Lin and Biyela 2005; Poppe et al. 2006; Mohapatra et al.
2008) and dihydrofolate reductase genes (dfr) (Mukherjee
and Chakraborty 2006) in surface water. ampC in surface
water biofilms (Schwartz et al. 2003) and bla genes in
estuarine water have also been detected (Henriques et al.
2006a).
ARGs in surface water and soils can leach to groundwater close to agriculture areas of animal production or
aquaculture. Tetracycline resistance genes encoding both
ribosomal protection proteins (tetO, Q, W, M, S, T, B(P),
and otrA; Chee-Sanford et al. 2001) and efflux pumps
(tetB, C, E, H, and Z; Aminov et al. 2002) have been
detected in the groundwater as far as 250 m downstream
from waste lagoons of swine farms. In a recent study, tetM,
408
O, Q, and W in wells near swine lagoons were quantified,

and the genes were then detected in groundwater downstream from manure lagoons (Mackie et al. 2006). Besides
in fresh waters, some ARGs associated with resistances to
aminoglycoside (Heuer et al. 2002) and chloramphenicol
(Dang et al. 2008) have also been detected in marine waters
with no evidence of being polluted.
Sediments
It is self-evident that ARGs in sediments are acquired from
water environments or produced for selection by the antibiotics present in the sediments. Sediments of aquaculture
farms are important antibiotic resistance regions where
various antimicrobials and ARGs are concentrated (Dalsgaard
et al. 2000; Agers and Petersen 2007).
Marine sediments perhaps can be considered as
natural reservoirs of tetracycline resistance gene tetM,
which has been found in various bacterial species in
sediments of Tokyo Bay, Sagami Bay, and the open
Pacific Ocean (Rahman et al. 2008). It was found that
numbers of oxytetracycline-resistant bacteria increased in
sediments around a marine aquaculture site after oxytetracycline therapy, and tetM was evident in both Grampositive and Gram-negative bacteria from various genera
in the sediments of the marine environment (Nonaka et al.
2007).
Various ARGs have also been identified in river sediments. Sulfonamide resistance genes including sulI, II, III,
and A were detected in the microorganisms of river water
and sediments (Pei et al. 2006). In rivers running through
pristine, urban, and agriculturally influenced areas, ARG
detection frequency in sediments was enhanced
corresponding to the increases in concentrations of various
antibiotic compounds (Yang and Carlson 2003; Pei et al.
2006). After a spatial monitoring of environmental bacteria
and genes, Suzuki et al. (2008) found that the detection
frequency of ribosomal protection protein genes (tetM, S,
and W) in sediments of the Mekong River watershed were
positively correlated with the occurrence rate of tetracycline-resistant bacteria in the same area.
Drinking water
Prevalence and resistance patterns of various microbial
genera isolated from drinking water distribution system
have been recently reported (Koksal et al. 2007; Ram et al.
2008). Multiple-antibiotic-resistant E. coli strains isolated
from drinking water was found to carry ARGs encoding
resistances to aminoglycoside, -lactam, tetracycline, and
trimethoprim-sulfamethoxazole (Alpay-Karaoglu et al.
2007; Cernat et al. 2007), as well as class 1 integrons
(Ozgumus et al. 2007).
In order to indicate possible ARGs transfer from

wastewater and surface water to the drinking water distribution network, Schwartz et al. (2003) and Obst et al. (2006)
investigated biofilms in hospital and municipal wastewater, as well as drinking water from river bank filtrate,
and found that vanA and ampC genes occurred not only
in wastewater biofilms but also in drinking water biofilms.
Florfenicol resistance gene floR and penicillin resistance
gene penA have also been found in Listeria monocytogenes isolated from drinking water in dairy farms
(Srinivasan et al. 2005). The appearance of potential
antibiotic resistances in drinking water distribution systems of some nations or regions requires increased
surveillance for risk assessment and prevention strategies
to protect public health.
ARGs horizontal transfer

ARGs emerge in aquatic environments as a direct result of
intensive use of antibiotics in hospitals, swine production
areas, and fish farms, and the genes in surface water and
groundwater around such areas can transfer antibiotic
resistance to the bacteria in drinking water or the food
chain (Chee-Sanford et al. 2001). Genetic mechanisms
involved in horizontal transfer of ARGs among environmental bacteria may include the following: (1) conjugative
transfer by mobile elements including plasmids, transposons, and integrons on plasmids or transposons; (2)
transformation by naked DNA, in the case of naturally
competent state of some bacteria, or an environmentally
induced competence such as the presence of calcium; and
(3) transduction by bacteriophage. Antibiotic resistance in
most environmental bacteria is due to the acquisition of
new genes, often associated with the mobile elements.
Plasmid is an initially discovered microbial mobile element
distributed in water environment, and STPs are considered as
important pools of the plasmids with transportable ARGs
(Szczepanowski et al. 2004; Tennstedt et al. 2005). Many
types of plasmids have been isolated from activated sludge
of STPs, which confer resistances to aminoglycoside
(Tennstedt et al. 2003), quinolone (Bnemann et al. 2006),
erythromycin (Schlter et al. 2007a), as well as multiple
drugs (Szczepanowski et al. 2005). Recently, Schlter et al.
(2007b) has reviewed the gene elements and functions of
IncP-1 plasmids isolated from wastewater treatment plants.
These self-transmissible plasmids are capable of transferring
to and replicating in a wide range of hosts and can encode
resistances to almost all types of clinically relevant
antibiotics (Szczepanowski et al. 2005; Schlter et al.
2007b).
Among the mobile elements, transposon and integron
also play important roles in horizontal transfer of environ-
mental ARGs. Previous reports demonstrated that transposons and integrons carrying various ARGs often occurred
in animal production or aquaculture areas (Schmidt et al.
2001; Moura et al. 2007; Akinbowale et al. 2007a; Jacobs
and Chenia 2007), STPs (Szczepanowski et al. 2004;
Tennstedt et al. 2005; da Silva et al. 2007; Taviani et al.
2008), surface waters (Poppe et al. 2006; Mukherjee and
Chakraborty 2006; Lin and Biyela 2005), and sediments
(Dalsgaard et al. 2000). The elements are not selfreplicating and must be carried by a phage or, more
typically, by a plasmid to move from one cell to another.
Insertion sequences, a type of small transposons, encode no
other functions but recombinase and transposase (Summers
2006). Transposons and insertion sequences often jump
randomly and occasionally on genome or plasmid, resulting
in new or multiple resistances (Naas 2007). Integron is not
capable of moving itself but can capture, integrate, and
express resistance gene cassettes in their variable regions
and can be transmitted via transposons and conjugative
plasmids (Fluit and Schmitz 1999; Alekshun and Levy
2007). Integrons with as many as nine ARGs, typically four
or five, are frequently found in clinical environments
(Crowley et al. 2008; Labuschagne et al. 2008), agricultural
wastewaters (Jacobs and Chenia 2007), urban wastewaters
(Tennstedt et al. 2003; da Silva et al. 2007), and even in the
waters not recently exposed to antibiotics (Park et al. 2003;
Obst et al. 2006).
Some physicochemical factors can influence the
dissemination of ARGs in aquatic environments. The
first factor contributing to the horizontal transfer of
ARGs is the selective pressure from ever-increasing
production and consumption of antibiotics for treatment
of disease and growth promotion. High selective pressure
facilitates the acquisition of ARGs, which may actually
increase the fitness of certain bacteria and allow the rapid
emergence and dissemination on a worldwide scale (Enne
et al. 2004; Luo et al. 2005). In addition, the presence of
antibiotics at low subinhibitory concentrations can accelerate horizontal transfer and dissemination of environmental
ARGs (Kmmerer 2004). It was found that keeping
antibiotic concentration at a subinhibitory level in the
mating medium significantly enhances conjugal transfer
mediated by plasmid or transposon in the environments
(Ohlsen et al. 2003; Hecht et al. 2007). Additionally,
Auerbach et al. (2007) found UV disinfection had no effect
on removal of tet genes in wastewater effluent, but loss rate
of tetM, O, P, and W in aquatic environments has a
significantly positive correlation to simulated sunlight
exposure (Engemann et al. 2006).
Many studies revealed that the co-selection took place in
the various environmental bacteria with metal and antibiotic
resistance (Berg et al. 2005; Stepanauskas et al. 2005; Wright
et al. 2006). Bacteria in metal-contaminated environments
409
appeared to be easier to obtain antibiotic resistance phenotypes than in control areas (Baker-Austin et al. 2006).
However, genetic mechanisms responsible for the coresistances occurring in the environments are poorly understood, since few researches have been carried out to
investigate ARGs in metal-contaminated environments,
though the experimental results of molecular genetics may
help to explain these phenomena. Rasmussen and Sorensen
(1998) found occurrence of conjugative plasmids carrying
tetracycline and mercury resistance genes was increased in a
contaminated site. Recently, a novel tetracycline resistance
gene, tetA(41), has been found in Serratia marcescens
isolated from a stream contaminated with heavy metals
(Thompson et al. 2007), which provides indirect evidence of
co-resistance. Wright et al. (2008) found that class 1
integrase gene was more abundant in the metal-exposed
environments than in control, and the selective pressures
shaped the structure of the gene cassette pool, indicating that
relative gene transfer potential is higher in the microbial
communities of the contaminated environments.
ARGs as emerging environmental pollutants

It was suggested by Rysz and Alvarez (2004) that ARGs
themselves could be considered as environmental pollutants, since they are widely distributed in various environmental compartments, including wastewater and STPs,
surface water, lagoon water of animal production areas,
aquaculture water, sediments and soil, groundwater, and
drinking water. Recently, Pruden et al. (2006) has also
pointed out that ARGs may be thought as emerging
contaminants, for the public health problems resulted
from the widespread dissemination of ARGs.
As many other chemical pollutants, for example,
persistent organic pollutants and heavy metals, ARGs are
well-known easy-to-get, hard-to-lose pollutants (Aminov
and Mackie 2007). Usually, antibiotic resistance bacteria
and genes emerge in the environments under the selection
pressure of some antibiotics, but the ARGs cannot be easily
removed from the polluted areas, even when the pressure
has disappeared (Salyers and Amabile-Cuevas 1997;
Aminov and Mackie 2007). This may be one explanation
why ARGs were often detected in antibiotic-free environments (Rahman et al. 2008). Potential public health
concerns for environmental ARGs carried by bacterial
pathogens were reviewed by Heuer et al. (2006) and Zhou
et al. (2007). Although the direct evidence about ARGs
transfer from the environments to human bodies is
unavailable, some studies still highlight the fact that ARGs
can spread and be exchanged among environmental microorganisms of different genera (Agers and Sandvang 2005;
Agers and Petersen 2007) and the organisms even within
410
completely different kingdoms (Rodrguez et al. 2006),

which is supposed to be a daunting public health risk
(Seveno et al. 2002; Alpay-Karaoglu et al. 2007).
Some efforts have to be made to reduce the possibility of
ARGs entering into and spread in the environments. The
most effective and direct approach is thought to be the
reasonable use of antibiotics in health protection and
agriculture production. New and effective wastewater
treatment processes are also needed to be developed to
improve removal efficiency of ARGs in STPs. Additionally,
feasibility of agricultural application of sludge or irrigation
with reclaimed wastewater has to be discussed thoroughly
considering possible introduction of ARGs to soil and
groundwater. Researches on transfer and degradation pathways of environmental ARGs and health risk assessment on
the genes may be performed to provide more scientific
information for responsible authorities to make up regulatory standards and guidelines to control environmental
dissemination of these pollutants.
Acknowledgements The authors wish to thank the Hong Kong
Research Grants Council for the financial support of this study (HKU
7129/05E and HKU 7195/06E).
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Appl Microbiol Biotechnol (2009) 82:397414

Antibiotic resistance genes in water environment

X.-X. Zhang : T. Zhang (*) : H. H. P. Fang

Appl Microbiol Biotechnol (2009) 82:397414

Types of environmental ARGs

antibiotics, which is genetically controlled by ARGs. The use

Table 1 Tetracycline resistance genes in water environments

Tetracycline efflux protein

Pseudomonas; microbial community

AS, DW, EW,

AS, DW, EW,

Szczepanowski et al. 2004; Agers and Sandvang

Macauley et al. 2007

Kobashi et al. 2007; Macauley et al. 2007

Agers and Sandvang 2005

Chee-Sanford et al. 2001; Pei et al. 2006

AS, EW, SW, US

Paenibacillus, Pseudoalteromonas, Shewanella,

Lactococcus and Vibrio; microbial community

AS, EW, NW,

Streptomycete; microbial community

AS, EW, NW, SD,

Appl Microbiol Biotechnol (2009) 82:397414

Table 2 Aminoglycoside resistance genes in water environments

Tennstedt et al. 2005; Mukherjee

Lee et al. 1998; Heuer et al. 2002

Aeromonas, Escherichia and Vibrio; AS, NW, SD,

Salmonella and Vibrio; Plasmids

Tennstedt et al. 2003; Henriques et al.

Cernat et al. 2007

The abbreviations of environmental sources are the same as those in Table 1

ARGs related to tetracycline

Appl Microbiol Biotechnol (2009) 82:397414

Table 3 Macrolide, chloramphenicol, and vancomycin resistance genes in water environments

Macrolide resistance genes

Hayes et al. 2005; Chen et al. 2007

Chloramphenicol resistance genes

DW, EW, NW, SW, UW

Heuer et al. 2004

The abbreviations of environmental sources are the same as those in Table 1

cell and keep the intercellular concentrations low to make

proved to be capable of interspecies transfer to Escherichia

Appl Microbiol Biotechnol (2009) 82:397414

Table 4 Sulphonamide and trimethoprim resistance genes in water environments

Dihydrofolate reductase encoding genes

Henriques et al. 2006a; Mukherjee and Chakraborty 2006;

DW, NW, SD, SW

The abbreviations of environmental sources are the same as those in Table 1.

The aac, aph, and ant genes are widely distributed in

Appl Microbiol Biotechnol (2009) 82:397414

Table 5 -Lactam and penicillin resistance genes in water environments

Environmental sourcea Function

DW, NW, SW, US

Aeromonas, Salmonella and Vibrio EW, SD, SW, US

Schwartz et al. 2003; Volkmann et al. 2004;

Antunes et al. 2006; Moura et al. 2007

Schwartz et al. 2003; Volkmann et al. 2004

Srinivasan et al. 2005

The abbreviations of environmental sources are the same as those in Table 1

of class 1 integron, can be disseminated and transferred

Appl Microbiol Biotechnol (2009) 82:397414

different -lactamases encoded by hundreds of ARGs (bla)

Molecular techniques for the detection