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Numidum Massiliense Gen. Nov., Sp. Nov., a New Member of the Bacillaceae Family Isolated from the Human Gut

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Numidum Massiliense Gen. Nov., Sp. Nov., a New Member of the Bacillaceae Family Isolated from the Human Gut Accepted Manuscript Numidum massiliense gen. nov., sp. nov., a new member of the Bacillaceae family isolated from the human gut Maryam Tidjani Alou, Thi-Tien Nguyen, Nicholas Armstrong, Jaishriram Rathored, Saber Khelaifia, Didier Raoult, Pierre-Edouard Fournier, Jean-Christophe Lagier PII: S2052-2975(16)30042-7 DOI: 10.1016/j.nmni.2016.05.009 Reference: NMNI 175 To appear in: New Microbes and New Infections Received Date: 15 April 2016 Revised Date: 10 May 2016 Accepted Date: 12 May 2016 Please cite this article as: Alou MT, Nguyen T-T, Armstrong N, Rathored J, Khelaifia S, Raoult D, Fournier P-E, Lagier J-C, Numidum massiliense gen. nov., sp. nov., a new member of the Bacillaceae family isolated from the human gut, New Microbes and New Infections (2016), doi: 10.1016/ j.nmni.2016.05.009. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT Numidum massiliense gen. nov., sp. nov., a new member of the Bacillaceae family isolated from the human gut Maryam Tidjani Alou 1, Thi-Tien Nguyen 1, Nicholas Armstrong 1, Jaishriram Rathored 1, Saber Khelaifia 1, Didier Raoult 1,2 , Pierre-Edouard Fournier 1, and Jean-Christophe Lagier 1.* 1Aix-Marseille Université, URMITE, UM63, CNRS7278, IRD198, Inserm 1095, Faculté de médecine, 27 Boulevard jean Moulin, 13385 Marseille cedex 05, France. 2Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia Running title: Numidum massiliense gen. nov., sp. nov *Corresponding author: Jean-Christophe Lagier MANUSCRIPT ([email protected]) ACCEPTED ACCEPTED MANUSCRIPT 1 Numidum massiliense gen. nov., sp. nov., a new member of the Bacillaceae family isolated 2 from the human gut 3 Abstract 4 Numidum massiliense gen. nov., sp. nov. strain mt3 T is the type strain of Numidum gen. nov., a 5 new genus within the family Bacillaceae. This strain was isolated from the fecal flora of a 6 Touareg male from Algeria. We describe here this Gram-positive facultative anaerobic rod 7 with its complete annotated genome sequence according to the taxono-genomics concept. Its 8 genome is 3,755,739 bp long and contains 3453 protein-coding genes and 64 RNA genes 9 including 8 rRNA genes. 10 Keywords: Numidum massiliense genome; culturomics; taxono-genomics MANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 11 Abbreviations 12 AGIOS: Average of Genomic Identity of Orthologous gene Sequences 13 bp: base pairs 14 COG: Clusters of Orthologous Groups 15 CSUR: Collection de souches de l’Unité des Rickettsies 16 DDH: DNA-DNA Hybridization 17 DSM: Deutsche Sammlung von Mikroorganismen 18 FAME: Fatty Acid Methyl Ester 19 GC/MS: Gaz Chromatography/Mass Spectrometry 20 kb: kilobases 21 MALDI-TOF MS: Matrix-assisted laser-desorption/ionization time-of-flight mass 22 spectrometry 23 ORF: Open Reading Frame MANUSCRIPT 24 TE buffer: Tris-EDTA buffer 25 SDS: sodium dodecyl sulfate 26 URMITE: Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes 27 28 29 30 ACCEPTED ACCEPTED MANUSCRIPT 31 1. Introduction 32 Several microbial ecosystems are harbored by the human body among which is the human gut 33 microbiota. This particular ecosystem is so vast that its cell count (10 14 cells) is evaluated at 34 ten times the number of human cells in the human body and its collective bacterial genome 35 size is 150 times superior to the human genome [1-4]. Over the years, with the evolution of 36 exploratory techniques of microbial ecosystems from culture to metagenomics, the gut 37 microbiota has been shown to be involved in many conditions such as obesity, inflammatory 38 bowel disease and irritable bowel disease [1]. It has also been shown to play key roles in 39 digestion, metabolic and immunological functions [1-3]. A better knowledge of the gut 40 microbiota’s composition is thus required for an improved understanding of its functions. 41 In order to extend the gut microbiota repertoire and bypass the “non-cultivable” bacteria 42 issue, the “culturomics” concept was developed in order to cultivate as exhaustively as 43 possible the viable population of a bacterial ecosystem;MANUSCRIPT it consists in the multiplication of 44 culture conditions, varying of media, temperature and atmosphere [5]. Using this technique, 45 strain mt3 T was isolated and identified as a previously unknown member of the Bacillaceae 46 family. Currently, there are 53 validated genera in the Bacillaceae family. This family was 47 created by Fisher in 1895 [6]. The genus Bacillus was described as its type genus. The genera 48 that belong to this family are rod shaped, mostly aerobic and facultative anaerobic bacteria. 49 They are found in various ecosystems like the human body, soil, water, air and other 50 environmental ecosystems [7]. 51 Bacterial classificationACCEPTED is currently based on a polyphasic approach with phenotypic and 52 genotypic characteristics such as DNA-DNA hybridization, G+C content, 16S rRNA sequence 53 similarity [8-10]. Nevertheless, this classification system has its limits, among which is the 54 high cost of the DNA-DNA hybridization technique and its low reproducibility [8; 11]. With 55 the recent development of genome sequencing technology [12], a new concept of bacterial ACCEPTED MANUSCRIPT 56 description was developed in our laboratory [13-17]. This “taxonogenomics” concept [18] 57 combines a proteomic description with the MALDI-TOF profile [19] associated with a 58 phenotypic description and the sequencing, annotation and comparison of the complete 59 genome of the new bacterial species [20]. 60 We hereby describe strain mt3 T, a new genus Numidum massiliense gen. nov., sp. nov. 61 (=CSUR P1305 = DSM 29571) a new member of the Bacillacaeae family, using this 62 “taxonogenomics” concept. 63 2. Materials and methods 64 2.1. Organism information 65 A stool sample was collected from a young healthy Targui male living in Algeria. Verbal 66 consent was obtained from the patient and the study was approved by the Institut Fédératif de 67 Recherche 48, Faculty of Medicine, Marseille, France, under agreement number 09-022. 68 2.2. Strain identification by MALDI-TOF MS andMANUSCRIPT 16S rRNA sequencing 69 The sample was cultured using the 18 culture condit ions of culturomics [21]. The colonies 70 were obtained by seeding on solid medium and were purified by subculture and identified 71 using MALDI-TOF MS [19; 22]. Colonies were deposited in duplicate on a MTP 96 MALDI- 72 TOF target plate (Brüker Daltonics, Leipzig, Germany), which was analyzed with a Microflex 73 spectrometer (Brüker Daltonics). The twelve spectra obtained were matched against the 74 references of the 7,567 bacteria contained in the database, by standard pattern matching (with 75 default parameter settings), with the MALDI BioTyper database software (version 2.0, 76 Brüker). An identificationACCEPTED score over 1.9 with a validated species allowed the identification at 77 the species level and a score under 1.7 did not enable any identification. When the 78 identification by MALDI-TOF MS failed, the 16S rRNA was sequenced [23]. Stackebrandt 79 and Ebers suggest similarity levels of 98.7% and 95% of the 16s rRNA sequence as a ACCEPTED MANUSCRIPT 80 threshold to define, respectively, a new species and a new genus without performing DNA- 81 DNA hybridization [24]. 82 2.3. Growth conditions 83 In order to determine our strain ideal growth conditions, different temperatures (25, 28, 37, 45 84 and 56°C) and atmospheres (aerobic, microerophilic and anaerobic) were tested. GENbag 85 Anaer and GENbag miroaer systems (BioMerieux, Marcy l’Etoile, France) were used to 86 respectively test anaerobic and microaerophilic growth. Aerobic growth was achieved with 87 and without 5% CO 2. 88 2.4. Morphologic, biochemical and antibiotic susceptibility testing 89 Gram staining, motility, catalase, oxidase and sporulation were tested as previously described 90 [21]. Biochemical description was performed using API 20 NE, ZYM and 50CH 91 (BioMerieux) according to the manufacturer’s instructions. Cellular FAME analysis was 92 performed by GC/MS. Two samples were preparedMANUSCRIPT with approximately 70 mg of bacterial 93 biomass per tube harvested from several culture plates. Fatty acid methyl esters were prepared 94 as described by Sasser [25]. GC/MS analyses were carried out as described before [26]. 95 Briefly, fatty acid methyl esters were separated using an Elite 5-MS column and monitored by 96 mass spectrometry (Clarus 500 - SQ 8 S, Perkin Elmer, Courtaboeuf, France). Spectral 97 database search was performed using MS Search 2.0 operated with the Standard Reference 98 Database 1A (NIST, Gaithersburg, USA) and the FAMEs mass spectral database (Wiley, 99 Chichester, UK). 100 Antibiotic susceptibilityACCEPTED testing was performed using disk diffusion method according to 101 EUCAST 2015 recommendations [27]. To perform the negative staining of strain mt3 T, 102 detection formvar coated grids were deposited on a 40 µL bacterial suspension drop, 103 incubated at 37°C for 30 minutes and on ammonium molybdate 1% for ten seconds. The dried ACCEPTED MANUSCRIPT 104 grids on blotted paper were observed with a Tecnai G20 transmission electron microscope 105 (FEI Company, Limeil-Brevannes, France). 106 2.5. Growth conditions and genomic DNA preparation 107 N. massiliense strain mt3 T (=CSUR P1305 =DSM 29571) was grown on 5% sheep blood- 108 enriched Columbia agar (BioMerieux) at 37°C in aerobic atmosphere. Bacteria grown on 109 three Petri dishes were harvested and resuspended in 4x100µL of TE buffer.
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