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Campylobacter Armoricus Sp. Nov., a Novel Member of the Campylobacter Lari Group Isolated from Surface Water and Stools from Humans with Enteric Infection

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Campylobacter Armoricus Sp. Nov., a Novel Member of the Campylobacter Lari Group Isolated from Surface Water and Stools from Humans with Enteric Infection 1 International Journal Of Systematic And Evolutionary Microbiology Archimer December 2019, Volume 69 Issue 12 Pages 3969-3979 https://doi.org/10.1099/ijsem.0.003836 https://archimer.ifremer.fr https://archimer.ifremer.fr/doc/00591/70346/ Campylobacter armoricus sp. nov., a novel member of the Campylobacter lari group isolated from surface water and stools from humans with enteric infection Boukerb Amine M. 1, Penny Christian 2, Serghine Joëlle 1, Walczak Cécile 2, Cauchie Henry-Michel 2, Miller William G. 3, Losch Serge 4, Ragimbeau Catherine 5, Mossong Joël 5, Mégraud Francis 6, 7, Lehours Philippe 6, 7, Bénéjat Lucie 7, Gourmelon Michèle 1, * 1 Ifremer, RBE-SGMM-LSEM, Laboratoire Santé Environnement Microbiologie, Plouzané, France 2 Luxembourg Institute of Science and Technology (LIST), Environmental Research and Innovation Department, Esch-sur-Alzette, Luxembourg 3 US Department of Agriculture, Produce Safety and Microbiology Research Unit, Agricultural Research Service, Albany, CA, USA 4 Laboratoire de Médecine Vétérinaire de l’Etat (LMVE), Veterinary Services Administration, Dudelange, Luxembourg 5 Laboratoire National de Santé (LNS), Epidemiology and Microbial Genomics, Dudelange, Luxembourg 6 INSERM, University of Bordeaux, UMR1053 Bordeaux Research In Translational Oncology, BaRITOn, Bordeaux, France 7 French National Reference Centre for Campylobacter and Helicobacter, Pellegrin University Hospital, Bordeaux, France * Corresponding author : Michèle Gourmelon, email address : [email protected] Abstract : During a study on the prevalence and diversity of members of the genus Campylobacter in a shellfish- harvesting area and its catchment in Brittany, France, six urease-positive isolates of members of the genus Campylobacter were recovered from surface water samples, as well as three isolates from stools of humans displaying enteric infection in the same period. These strains were initially identified as members of the Campylobacter lari group by MALDI-TOF mass spectrometry and placed into a distinct group in the genus Campylobacter, following atpA gene sequence analysis based on whole-genome sequencing data. This taxonomic position was confirmed by phylogenetic analysis of the 16S rRNA, rpoB and hsp60 (groEL) loci, and an analysis of the core genome that provided an improved phylogenetic resolution. The average nucleotide identity between the representative strain CA656T (CCUG 73571T=CIP 111675T) and the type strain of the most closely related species Campylobacter ornithocola WBE38T was 88.5 %. The strains were found to be microaerobic and anaerobic, motile, non-spore- forming, Gram-stain-negative, spiral-shaped bacteria that exhibit catalase, oxidase and urease activities but not nitrate reduction. This study demonstrates clearly that the nine isolates represent a novel species within the C. lari group, for which the name Campylobacter armoricus is proposed. Here, we present phenotypic and morphological features of the nine strains and the description of their genome sequences. Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site. 2 The proposed type strain CA656T has a 1.589 Mbp chromosome with a DNA G+C content of 28.5 mol% and encodes 1588 predicted coding sequences, 38 tRNAs, and 3 rRNA operons. Keywords : Campylobacter, novel species, surface water, coastal catchment, human gastroenteritis, C. lari group, whole genorne sequence Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site. ABBREVIATIONS: ANIb, average nucleotide identity based on BLAST; CA-SFM, Comité de l'Antibiogramme de la Société Française de Microbiologie; CFA, campyfoodagar; EUCAST, European committee for antimicrobial and susceptibility testing; HSP, high-scoring segment pairs; isDDH, in silico DNA-DNA hybridization; LPSN, list of prokaryotic names with standing in nomenclature; MALDI-TOF, matrix assisted laser desorption ionization-time of flight; MH-F, Mueller-Hinton agar supplemented with 5% defibrinated horse blood; MIC, minimum inhibitory concentrations; MSP, main spectrum profile; NRC, French National Reference Center for Campylobacter; TCS, trypto-casein-soy; TSA, tryptic soy agar; TSH, tryptic soy agar supplemented with 5% horse blood; TTC, triphenyltetrazolium chloride. ACCESSION NUMBERS: The DDBJ/ENA/GenBank accession numbers for the whole genome assemblies of the type strain CA656T and strains CA592, CA594, CA639, CA658, CA663, CA1650 (2014/2961), CA1665 (2014/0226h) and CA1670 (2016/0860h) are SBEZ00000000, SBFC00000000, SBFB00000000, SBFA00000000, SBEY00000000, SBEX00000000, SBEW00000000, SBEV00000000, SBEU00000000, respectively. The GenBank accession number of the 16S rRNA gene sequence of CA656T is MK632223. Campylobacter infections are recurrently confirmed as the world’s leading cause of bacterial gastroenteritis [1]. In the European Union, campylobacteriosis is the most frequently reported food-borne illness, with over 246000 human cases a year [2]. In addition to the major poultry- related transmission route, numerous other domestic animal and wildlife sources have been identified [3]. The number and diversity of species of the genus Campylobacter transiting through animal and environmental compartments is important [1, 4, 5], and emphasizes the need to adopt an integrated One-Health approach in Campylobacter epidemiology and risk assessment [6]. Currently, the genus Campylobacter encompasses 31 species, 11 subspecies and three biovars, according to the list of prokaryotic names with standing in nomenclature (LPSN; http://www.bacterio.net/campylobacter.html), accessed on July 30th, 2019). Thermotolerant Campylobacter, such as Campylobacter jejuni, Campylobacter coli and Campylobacter lari, are the most commonly-implicated species in Campylobacter infections [2]. The purpose of the present One-Health-based study, conducted from 2013 to 2016, was to investigate the importance of the water-related transmission and recirculation of isolates of members of the genus Campylobacter from the C. lari group [7] in the La Fresnaye coastal catchment area located in the north-eastern part of Brittany (Côtes d’Armor department, France). The La Fresnaye catchment corresponds to a 121 km2 area, characterized by intensive livestock (cattle and swine) and poultry farming, with a human population of about 6900 inhabitants [8, 9]. Specific focus was given to the presence of the bacteria in shellfish-producing areas downstream of the coastal catchment, the diversity found in the catchment’s rivers and seawater, the faecal carriage among wildfowl and the related incidence in the French human population. In an evaluation of the prevalence of species of the genus Campylobacter in three French coastal catchments, including the La Fresnaye catchment, species of the genus Campylobacter were recovered from 58.3% (n=228) of water samples and 26.6% (n=238) of shellfish samples [9]. C. lari was the most frequently isolated species in shellfish, with 26.4% of samples positive for this species, while it was isolated in 10.6% of surface water samples [9]. Among a collection of more than 250 C. lari group strains from environmental samples and human stools, special interest was given to nine isolates. Although these strains were initially identified as C. lari by mass spectrometry using a MALDI-TOF mass spectrometer (MALDI- TOF Bruker Microflex), a preliminary atpA phylogenetic analysis indicated that they formed a new clade within the C. lari group. Six of these isolates were obtained from three distinct river water samples collected at the outlet of one of the four main rivers of the La Fresnaye catchment named “Le Rat” (10.5 km long and a subcatchment area of 19.2 km2) at three sampling dates in 2014 (January 6th, two isolates; February 4th, three isolates; and March 4th, one isolate). These river water strains (CA592, CA594, CA639, CA656T, CA658, and CA663) were isolated using the ISO-10272:2016 method or by a passive filtration method. Colonies suspected to be members of the genus Campylobacter were confirmed by a qPCR assay targeting the 16S rRNA gene [9, 10]. Additionally, three clinical isolates (CA1650, CA1665, and CA1670) were recovered from human stool samples collected in 2014 and 2016 in three laboratories participating in the network of the French National Reference Centre for Campylobacters. They were located in three departments geographically distant from the La Fresnaye catchment area [October 3, 2014 in the Ille-et-Vilaine department (69-year-old male); April 8, 2014 in the Seine department (41-year-old female); and September 14, 2016 in the Vendée department (75-year- old male)]. These nine isolates were subjected to a thorough genomic and phenotypic characterization approach, according to the minimal standards recommended for describing novel species of the genus Campylobacter [11]. The morphology, presence of flagella and cell size of C. armoricus were determined by transmission electron microscopy. Bacteria were scraped and introduced into a fixative solution of 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.4) and incubated for 1 h at room temperature. After centrifugation for 3 min at 2350 g, pellets were mixed/suspended in 500 μl of 0.1 M sodium cacodylate buffer (pH 7.4). A 10 μl sample of bacterial suspension was adsorbed onto
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