The pollution level of the blaOXA-58 carbapenemase gene in coastal water and its host bacteria characteristics☆
Graphical abstract
Introduction
Carbapenems possess a broad spectrum of activity and great stability to almost all β-lactamases that were invented on the basis of thiomycin (Woznica et al., 2010). They can acylate penicillin-binding protein (PBPs), inhibiting the formation of the peptidoglycan, which leads to cell death (Galal et al., 2010). Carbapenems displayed inhibitory microbiological activity against many infectious bacteria, such as Pseudomonas aeruginosa, Bacteroides fragilis, Staphylococcus aureus and Streptococci, that are often used as “antibiotics of last resort” to treat multidrug resistance (Kattan et al., 2008). However, the widespread use of carbapenems promotes a selection pressure for carbapenem resistance in bacteria (Kumarasamy et al., 2010). β-lactamases are a major antibiotic resistance mechanism employed by bacteria, among which carbapenemases have the ability to hydrolyze carbapenems (Papp-Wallace et al., 2011). Carbapenemases are divided into 3 classes: the Ambler class A (e.g., KPC and GES enzymes), class B (e.g., VIM, IMP, and NDM β-lactamases) and class D (e.g., OXA-23, -24/-40, −48, −51, and −58) (Potter et al., 2016). Carbapenemase genes were mainly found in the bacteria causing difficult-to-treat infections, including Enterobacteriaceae, Acinetobacter baumannii, and P. aeruginosa (Diene and Rolain, 2014). Some studies showed that infections causing by carbapenem resistant Enterobacteriaceae and A. baumannii were associated with higher death rates (Lemos et al., 2014; Martin et al., 2016).
The first carbapenemase gene was discovered in an A. baumannii isolated from a patient in Royal Hospital, Edinburgh, UK and was identified as the blaOXA-23 gene in a later study (Paton et al., 1993). Since then, a large variety of carbapenemase genes (e.g. blaSME, blaIMP, blaVIM, blaGES, blaKPC, blaOXA-48, and blaNDM) have been identified in hospital environment (Lauretti et al., 1999; Naas et al., 1994; Osano et al., 1994; Poirel et al., 2000, 2004; Rasmussen et al., 1996; Toleman et al., 2002; Yigit et al., 2001; Yong et al., 2009). Notably, a carbapenem resistant Streptomyces sp. CN229 was isolated in soil samples from the natural environment in Tunisia in 2007, although the carbapenemase genes were not identified (Lazim et al., 2007). blaOXA-23 was the first carbapenemase gene detected in an A. baumannii isolated from its natural environment in 2010 (Girlich et al., 2010). Some carbapenemase-producing isolates have been successively recovered from the non-clinical environment, including water samples (groundwater, seawater, waste water and drinking water) (Fernando et al., 2016; Galler et al., 2014; Nascimento et al., 2017; Tafoukt et al., 2017) and sediment samples from the river and waste water treatment plant (Devarajan et al., 2017; Yang et al., 2017). The widespread nature of these genes would be a serious ecological and human health threat (Christophy et al., 2017).
blaOXA-58-types are one of three major subfamilies in class D carbapenemase-encoding genes (Mendes et al., 2009). It was detected in a hospital environment in China, India and Mediterranean countries and was always reported in Acinetobacter spp. (Mendes et al., 2009; Djahmi et al., 2014; Gur et al., 2008). The blaOXA-58 gene has been found located on transferable plasmids and has the ability to transfer to other bacteria (Poirel et al., 2005). However, there are rare data on the abundance of blaOXA-58 gene in the non-clinical environment. To the best of our knowledge, this gene was only found in feces samples of pigeons and chicken (Morakchi et al., 2017; Vergara et al., 2017), as well as the body of some animals, such as black necked swan (Narciso et al., 2017), dog, rabbit and cat (Klotz et al., 2107). Furthermore, blaOXA-58 gene has been found in Acinetobacter spp. in coastal seawater in 2017 for the first time (Paschoal et al., 2017).
The coastal area is closely related to human beings and may exert an impact on human health when people recreate or work in coastal regions. Moreover, seawater could facilitate the propagation of antibiotic resistance genes (ARGs) and could lead to global pollution (Niu et al., 2016). Carbapenem resistant bacteria were first investigated in the coastal water in 2013. The study showed that 40% of the marine isolates were resistant to meropenem (Moore et al., 2013). Then, a study of ARGs in Enterobacteriaceae from coastal seawater samples around Berlenga Island was conducted, in which researchers identified 27 types of ARGs but without carbapenemase genes (Alves et al., 2014). In the same year, blaKPC and blaGES were detected in Aeromonas and Enterobacteriaceae from Guanabara Bay Beach (Montezzi et al., 2015). blaVCC, blaKPC and blaNDM were identified in Vibrio and Enterobacteriaceae, which were isolated from German nearshore waters and a beach in Brazil, respectively (Campana et al., 2017; Hammerl et al., 2017; Sellera et al., 2017). Two hundred and ninety-five types of ARGs were investigated in the coastal area of China in 2016 by using high-throughput quantitative polymerase chain reaction, in which 4 types of carbapenemase genes (blaGES, blaIMP, blaVIM and blaPER) were detected (Zhu et al., 2017). In 2007, eleven carbapenemase genes were found in 8 bacterial genus from coastal seawater, including Acinetobacter spp., Aeromonas spp., Citrobacter spp., Enterobacter spp., Klebsiella spp., Kluyvera spp., Pseudomonas spp. and Serratia spp. (Paschoal et al., 2017).
However, few studies focused on the carbapenemase genes in the coastal environment compared to those in the fresh water environment (Table S1). Some genes encoding resistance to carbapenems (e.g., blaIMP, blaOXA-51, blaOXA-58), which were frequently found in the terrestrial environment, were rarely detected in the coastal area. Additionally, previous research paid more attention to specific bacteria, such as Enterobacteriaceae, Aeromonas and Pseudomonas.
Although it is necessary to know the distribution of carbapenemase genes in the environment, there were very few reports on carbapenemase genes pollution in the coastal area, especially in China. Thus, we sampled at Bohai Bay to investigate the prevalence and characteristics of carbapenemase genes in the coastal area, as well as provide more information about the influence of carbapenemase resistance on the coastal environmental.
Section snippets
Study site and sample collection
Coastal seawater was sampled in November 2017, from Bohai Bay located in Tianjin, China (the details of the bay are shown in SI-1). Eight sampling points in the coastal area were selected (Fig. 1). The sampling points are located away from the Tianjin Beitang estuary, approximately 0 m, 1000 m, 2500 m, 4500 m, 6500 m, 8500 m, 10500 m and 12500 m. A sewage outlet is located between sampling points 4 and 5. Triplicate samples in each site were collected and combined in sterile bottles (3 L) from
Prevalence of imipenem-resistant bacteria and genes
Imipenem-resistant bacteria were found in all sampling points in this study, whose number ranged from 230 to 4100 (±21–377) CFU/mL in seawater (Table 1). The highest abundance of imipenem-resistant bacteria was observed at S1 and S2, and the lowest abundance was detected at S8, which is the farthest site from the estuary. We found a decreasing trend for the abundance of imipenem-resistant bacteria determined by plate counts along the river flow from the estuary to its receiving sea. The Pearson
Conclusions
Comparing with the previous studies, we found higher numbers of carbapenem resistant bacteria in coastal area, which may have ecological and public health implications. blaOXA-58 gene was detected in 9 bacterial genera, including marine indigenous bacteria. Moreover, the host of blaOXA-58 took up a larg percentage of carbapenemase-resistant bacteria living in coastal area. All isolates in this study have multidrug-resistant phenotypes and most of OXA-58-producing isolates have a wide
Acknowledgement
This work was supported by the National Natural Science Foundation of China (41831287), and the Fundamental Research Funds for the Central Universities of China.
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This paper has been recommended for acceptance by Klaus Kummerer.
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R. Xin and K. Zhang contributed equally to this work.