Bacterial Diversity and Antibiotic Susceptibility of Sparus aurata from Aquaculture

Abstract

In a world where the population continues to increase and the volume of fishing catches stagnates or even falls, the aquaculture sector has great growth potential. This study aimed to contribute to the depth of knowledge of the diversity of bacterial species found in Sparus aurata collected from a fish farm and to understand which profiles of diminished susceptibility to antibiotics would be found in these bacteria that might be disseminated in the environment. One hundred thirty-six bacterial strains were recovered from the S. aurata samples. These strains belonged to Bacillaceae, Bacillales Family XII. Incertae Sedis, Comamonadaceae, Enterobacteriaceae, Enterococcaceae, Erwiniaceae, Micrococcaceae, Pseudomonadaceae and Staphylococcaceae families. Enterobacter sp. was more frequently found in gills, intestine and skin groups than in muscle groups (p ≤ 0.01). Antibiotic susceptibility tests found that non-susceptibility to phenicols was significantly higher in gills, intestine and skin samples (45%) than in muscle samples (24%) (p ≤ 0.01) and was the most frequently found non-susceptibility in both groups of samples. The group of Enterobacteriaceae from muscles presented less decreased susceptibility to florfenicol (44%) than in the group of gills, intestine and skin samples (76%). We found decreased susceptibilities to β-lactams and glycopeptides in the Bacillaceae family, to quinolones and mupirocin in the Staphylococcaceae family, and mostly to β-lactams, phenicols and quinolones in the Enterobacteriaceae and Pseudomonadaceae families. Seven Enterobacter spp. and five Pseudomonas spp. strains showed non-susceptibility to ertapenem and meropenem, respectively, which is of concern because they are antibiotics used as a last resort in serious clinical infections. To our knowledge, this is the first description of species Exiguobacterium acetylicum, Klebsiella michiganensis, Lelliottia sp. and Pantoea vagans associated with S. aurata (excluding cases where these bacteria are used as probiotics) and of plasmid-mediated quinolone resistance qnrB19-producing Leclercia adecarboxylata strain. The non-synonymous G385T and C402A mutations at parC gene (within quinolone resistance-determining regions) were also identified in a Klebsiella pneumoniae, revealing decreased susceptibility to ciprofloxacin. In this study, we found not only bacteria from the natural microbiota of fish but also pathogenic bacteria associated with fish and humans. Several antibiotics for which decreased susceptibility was found here are integrated into the World Health Organization list of “critically important antimicrobials” and “highly important antimicrobials” for human medicine.

Antibiotic-Resistant Bacteria in Aquaculture and Climate Change: A Challenge for Health in the Mediterranean Area

“…strains resulted in resistance to ertapenem and meropenem, antibiotics used in serious clinical infections. Several antibiotics for which resistance was found in these isolates appear in the World Health Organization list of “critically important antimicrobials” and “highly important antimicrobials” for human medicine [ 126 ]. In Mediterranean aquaculture, and in particular the Greek fish farm facilities, several registered antibiotics are currently available against bacterial infections, including tetracyclines, quinolones, and fluoroquinolones, potential sulfa, penicillin, and chloramphenicol derivatives.…”

Assessing the Bacterial Community Composition of Bivalve Mollusks Collected in Aquaculture Farms and Respective Susceptibility to Antibiotics

“…Information about the frequency and pathogenicity of other genera found in this study in bivalve mollusks is scarce. However, there are several studies reporting human infections caused by all seven genera described above, namely wound infections, foodborne diseases (by ingestion of raw seafood), myonecrosis, septicemia, necrotizing fasciitis, empyema, bacteremia, endocarditis, severe respiratory, urinary and biliary tract infections, meningitis, and keratitis [ 9 , 18 , 19 , 20 , 22 , 23 , 24 , 25 , 26 , 27 ].…”

“…The genera Enterobacter , Enterococcus , Klebsiella , Proteus , Providencia, and Staphylococcus , as well as the species from Citrobacter freundii complex, Escherichia coli , Morganella morganii , Shewanella algae and Vagococcus fluvialis , found in this study, were already reported in bivalve mollusks (especially clams, mussels and oysters) [ 12 , 13 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 ]. These groups of bacteria, some of which are fish pathogens, are commonly found in aquatic environments [ 12 , 25 , 34 , 35 , 37 , 38 ]. All these bacteria were already associated with human infections, such as ear and eye infections, osteomyelitis, infective arthritis, endocarditis, bacteremia, meningitis, intestinal and urinary tract infections, brain abscess, peritonitis, enteritis and septicemia, and some are recognized as important agents in nosocomial infections [ 12 , 13 , 34 , 37 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 ].…”

“…Non-commensal bacteria of bivalve mollusks such as Enterobacter spp., Enterococcus faecalis, Enterococcus faecium, E. coli, Klebsiella aerogenes, K. pneumoniae, M. osloensis, M. morganii, and Providencia rettgeri could be indicators of fecal contamination, since these bacteria are widely found in the gastrointestinal tract of humans and several other animals [ 13 , 25 , 32 , 34 , 35 , 40 , 46 , 48 , 51 ]. These and other bacteria can enter aquaculture farms through runoff from land (especially during periods of high precipitation), sewage, maritime traffic and birds or marine mammals.…”

“…Decreased susceptibility to β-lactams was also found in the present study. This antibiotic class is frequently used in aquaculture in several countries [ 25 ] and high resistance rates are usually observed in bivalve mollusks (especially regarding amoxicillin), often associated with bla TEM and bla CTX-M [ 13 ]. In our study, we also detected the bla TEM-1 gene in eight multidrug resistant E. coli strains with decreased susceptibility to amoxicillin, amoxicillin/clavulanic acid and/or ceftazidime.…”