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Bats As Reservoirs of Antibiotic Resistance Determinants a Survey Infection, Genetics and Evolution 70 (2019) 107–113 Contents lists available at ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid Research paper Bats as reservoirs of antibiotic resistance determinants: A survey of class 1 integrons in Grey-headed Flying Foxes (Pteropus poliocephalus) T ⁎ Fiona McDougalla, , Wayne Boardmanb, Michael Gillingsa, Michelle Powera a Department of Biological Sciences, Macquarie University, NSW 2109, Australia b School of Animal and Veterinary Sciences, University of Adelaide, SA 5371, Australia ARTICLE INFO ABSTRACT Keywords: Increasing reports of antimicrobial resistance in wildlife highlight the significance of a One Health approach to Antimicrobial resistance managing resistance. We investigated the prevalence and diversity of class 1 integrons, a genetic determinant of Bats resistance, in grey-headed flying foxes, a large fruit bat species belonging to the order Chiroptera. Class 1 in- Integron tegrons were detected in both wild flying foxes (5.3%) and captive flying foxes (41.2%) housed in wildlife One Health rehabilitation facilities. Genes encoding resistance to aminoglycosides, trimethoprim and beta-lactams, and Qac Resistome efflux pumps were detected. Analysis of conserved integron elements and gene cassette arrays indicate the Reverse zoonosis direction of integron transfer is from humans to flying foxes. The detection of two novel gene cassette arrays (5′CS-qacH-aacA34-blaOXA-21-3′CS and 5′CS-qacF-3′CS strongly suggests acquisition of genes from the environ- mental resistome into class 1 integrons within the flying fox microbiota. The dynamics of class 1 integrons in flying foxes indicates bats have a role in the emergence of novel antibiotic resistance determinants. 1. Introduction of free mobile gene cassettes into a primary recombination site (attI1). Each gene cassette within the array is separated by secondary re- Antimicrobial resistance (AMR) is a global issue that is no longer combination sites (attC). A promoter (Pc) then drives expression of the entirely confined to human health contexts. Increasing reports of AMR inserted gene cassettes, which in clinical pathogens usually encode in wildlife highlight the need to understand the ecology of resistant antibiotic resistance genes (Hall and Collis, 1995). IntI1 also mediates bacteria in wildlife settings (Greig et al., 2015). Dissemination of re- the excision of gene cassettes from the array, producing free gene cas- sistance via the microbiota of wild animals is clearly an issue for the settes. The IntI1 mediated recombination system allows class 1 in- management of resistance. Strategies aimed at combatting anti- tegrons to capture, remove and shuffle gene cassettes (Hall and Collis, microbial resistance stress the need for a multidisciplinary and colla- 1995). The association of class 1 integrons with transposons and plas- borative “One Health” approach, addressing interactions between mids allows for transfer of integrons between different bacterial hosts people, domestic animals, wildlife and the environment (FAO-OIE- by horizontal gene transfer (Gillings et al., 2008). WHO, 2010). However, current antimicrobial resistance surveillance Wildlife can acquire antibiotic resistant bacteria from human and programs typically focus on humans and domestic animals, and rarely domestic animal effluent, wastewater treatment plants, and aqua- extend to wildlife. culture operations (Arnold et al., 2016). Antibiotics released into the The rapid spread of AMR has been facilitated by mobile genetic environment can apply selective pressure, promoting the fixation of elements, such as plasmids, transposons, and integron gene cassettes. lateral transfer events in environmental bacterial communities and in One type of integron, the class 1 integron, is predominantly responsible wildlife microbiota (Allen et al., 2010; Finley et al., 2013). Bacteria that for spreading antibiotic resistance to most Gram-negative bacteria of harbor class 1 integrons have been detected in numerous wildlife spe- clinical importance (Stokes and Gillings, 2011). Class 1 integrons con- cies, many of which are closely associated with aquatic environments tain a 5′ conserved segment (5′CS) encoding an integrase gene (intI1), (such as black-headed gull Larus ridibundus, lesser flamingo Phoenico- and a variable number of gene cassettes, which form a gene cassette naias minor, Australian sea lion Neophoca cinereal and Eurasian otter array. The 3′ conserved segment (3′CS) commonly contains the qacE Lutra lutra), suggesting water as a primary vector (Alonso et al., 2017a; and sul1 genes (qacEΔ1-sul1). IntI1 mediates site-specific recombination Delport et al., 2015; Dolejska et al., 2009; Fulham et al., 2018; Sato ⁎ Corresponding author at: E8A, 14 Eastern Rd, Department of Biological Sciences, Macquarie University, NSW 2109, Australia. E-mail addresses: fi[email protected] (F. McDougall), [email protected] (W. Boardman), [email protected] (M. Gillings), [email protected] (M. Power). https://doi.org/10.1016/j.meegid.2019.02.022 Received 1 January 2019; Received in revised form 17 February 2019; Accepted 20 February 2019 Available online 21 February 2019 1567-1348/ © 2019 Elsevier B.V. All rights reserved. F. McDougall, et al. Infection, Genetics and Evolution 70 (2019) 107–113 et al., 2009). How free-living terrestrial wildlife species (such as Eur- IntI1 positive samples were then amplified using primers HS458 and opean mouflon Ovis orientalis musimon, wild boar Sus scrofa, black kite HS459 (Table 1)(Holmes et al., 2003), using cycling conditions of 94 °C Milvus migrans, or monitor lizards Varanus spp.) acquire antibiotic re- 3 min; 35 cycles 94 °C 30 s, 55 °C 30 s, 72 °C 1 min 30 s; 72 °C 5 min sistant bacteria is less clear (Alonso et al., 2017a; Alonso et al., 2017b; (Waldron and Gillings, 2015). HS458 and HS459 target the conserved Fischer et al., 2013; Waturangi et al., 2003). Class 1 integrons detected attI1 and 3′ qacEΔ1 regions. This amplifies the entire gene cassette in aquatic and terrestrial wildlife are frequently identical to those array, and amplicons vary in size depending on the number and type of identified in human or domestic animal microbiota (Partridge et al., gene cassettes present in the array. Samples can contain multiple cas- 2009; Stokes and Gillings, 2011). Given the number of class 1 integrons sette arrays of differing sizes, indicating the carriage of integrons con- released by humans and their domestic animals each day, the dominant taining different genes in the cassette array. HS458/HS459 amplicons direction of transfer is clearly towards wild species, and into the en- of low intensity were excluded from further analysis. vironment (Gillings, 2018; Zhu et al., 2017). Proximity to humans and domestic animals strongly influences the 2.3. DNA purification, cloning and sequencing prevalence of class 1 integrons in wildlife (Skurnik et al., 2006). The occurrence of AMR in captive wildlife is considerably greater than their Gene cassette array amplicons were purified using the MinElute PCR free-living counterparts (Delport et al., 2015; Kinjo et al., 1992; Power Purification Kit (QIAGEN, Hilden, Germany), and those with single et al., 2013). Understanding the potential flux of resistance genes and bands were sequenced directly using primers HS458 and HS459. For integrons through various environmental compartments and wild spe- large amplicons (≥1200 bp) the internal sequencing primer HS320 cies requires a study organism with a wide-ranging distribution that (Table 1)(Holmes et al., 2003) was used to generate overlapping intersects with urban environments. One animal that fulfils these re- fragments. For one very large amplicon (≥2200 bp) three additional quirements is the grey-headed flying fox (Pteropus poliocephalus), a large internal sequencing primers (FF509F, FF710R and FF1340R) (Table 1) species of fruit bat endemic to Australia. The grey-headed flying fox is were designed to obtain full length sequences. found in coastal regions of Eastern Australia, extending from Ingham in PCR products containing multiple gene cassette arrays underwent Queensland to Adelaide in South Australia (Eby, 2008). The species is DNA cloning using the TOPO® TA Cloning® Kit with Vector pCR™4- highly mobile with bats regularly travelling > 50 km each night to TOPO® and One Shot® TOP10 E. coli cells (Invitrogen, Carlsbad, CA, reach foraging sites (Eby, 1991), or moving hundreds of kilometres USA). Between eight and sixteen colonies of transformed E. coli were between camps (Eby, 1991; Roberts et al., 2012). Each year, thousands selected from each cloned sample and DNA from cell lysate (95 °C 5 min of injured and orphaned grey-headed flying foxes are rescued, re- and centrifugation; RCF = 12,000, 5 min, 22 °C) was screened using habilitated and released by wildlife care groups, providing opportunity HS458 and HS459 PCR as above. Amplicons of variable sizes were se- for exposure to human associated microorganisms, including antibiotic lected for sequencing. Alternatively, amplicon bands were excised from resistant bacteria. an agarose gel and purified using the Wizard® SV Gel and PCR Clean-Up To understand the potential for class 1 integrons to spread from System (Promega, Madison, WI, USA), then sequenced as above. human dominated ecosystems into wild animals we examined the DNA sequencing was performed at the Australian Genome Research prevalence and diversity of integrons in grey-headed flying foxes. We Facility
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