Antimicrobial resistance and antimicrobial resistance
genes in marine bacteria from salmon aquaculture and
non-aquaculture sites
Syed Q. A. Shah,
1
Felipe C. Cabello,
2
Trine M. L’Abée-Lund,
1
Alexandra Tomova,
2
Henry P. Godfrey,
3
Alejandro H. Buschmann
4
and
Henning Sørum
1
*
1
Norwegian University of Life Sciences, Ullevålsvein 72,
Oslo, Norway.
Departments of
2
Microbiology and Immunology and
3
Pathology, New York Medical College, Valhalla, NY
10595, USA.
4
Centro i-mar, Universidad de Los Lagos, Puerto Montt,
Chile.
Summary
Antimicrobial resistance (AR) detected by disc diffu-
sion and antimicrobial resistance genes detected by
DNA hybridization and polymerase chain reaction
with amplicon sequencing were studied in 124 marine
bacterial isolates from a Chilean salmon aquaculture
site and 76 from a site without aquaculture 8 km
distant. Resistance to one or more antimicrobials was
present in 81% of the isolates regardless of site.
Resistance to tetracycline was most commonly
encoded by tetA and tetG; to trimethoprim, by dfrA1,
dfrA5 and dfrA12; to sulfamethizole, by sul1 and sul2;
to amoxicillin, by bla
TEM; and to streptomycin, by
strA-strB. Integron integrase intl1 was detected in 14
sul1-positive isolates, associated with aad9 gene cas-
settes in two from the aquaculture site. intl2 Integrase
was only detected in three dfrA1-positive isolates
from the aquaculture site and was not associated with
gene cassettes in any. Of nine isolates tested for con-
jugation, two from the aquaculture site transferred AR
determinants to Escherichia coli. High levels of AR in
marine sediments from aquaculture and non-
aquaculture sites suggest that dispersion of the large
amounts of antimicrobials used in Chilean salmon
aquaculture has created selective pressure in areas
of the marine environment far removed from the initial
site of use of these agents.
Introduction
Chile is the second largest producer of farmed salmon
and trout in the world after Norway (FAO, 2011). Infections
by bacteria, parasites, fungi and viruses are a frequent
cause of morbidity and mortality in intensive salmon aqua-
culture in Chile, with concomitant decreases in production
and income (Asche et al., 2010; Cabello et al., 2013).
Efforts to increase productivity by high-stocking densities
favour the emergence of infections and facilitate the free
dissemination of epizootic pathogens (Asche et al., 2010;
Ibieta et al., 2011). While infection control in salmon aqua-
culture by vaccination and improved hygienic conditions
provides the best long-term approach (Markestad and
Grave, 1997; Berg et al., 2006; Bravo and Midtlyng, 2007;
Midtlyng et al., 2011), antimicrobials are the current
primary tools for prevention and treatment of bacterial
infections (Grave et al., 1999; Sørum, 2006). In Chile, a
lack of use of the few available vaccines, the continuous
high prevalence of bacterial infections such as salmon
rickettsial syndrome caused by Piscirickettsia salmonis,
the presence of antimicrobial-resistant pathogens and the
emergence of new pathogens has stimulated the use of
large quantities of antimicrobials (Asche et al., 2010;
Ibieta et al., 2011; Millanao et al., 2011; Cabello et al.,
2013).
Medicated feed and rarely, bath immersion, are com-
monly used in salmon farming to prevent bacterial infec-
tions (Sørum, 2006; Smith et al., 2009b). Some of the
feed is not ingested, and its antimicrobial activity, along
with that of metabolized and unmetabolized antimicrobials
in fish urine and faeces, ends up in the surrounding envi-
ronment (Cabello et al., 2013). Passage of antimicrobials
into the environment can select for resistant bacteria and
increase horizontal gene transfer (HGT) and genetic
recombination of antimicrobial resistance genes (ARG).
There appears to be an unimpeded flow of ARG between
the resistome of environmental, animal and human bac-
teria, so that increased antimicrobial resistance (AR) in
the aquatic environment has the potential to introduce AR
determinants into the resistomes of piscine and human
Received 1 October, 2013; revised 29 January, 2014; accepted 31
January, 2014. *For correspondence. E-mail henning.sorum@
nmbu.no; Tel. +47 22964770; Fax +47 22964818.
Environmental Microbiology (2014) 16(5), 1310–1320 doi:10.1111/1462-2920.12421
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd