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Ecological Structuring of Temperate Bacteriophages in the Inflammatory Bowel Disease-Affected Gut Hiroki Nishiyama, Hisashi Endo, Romain Blanc-Mathieu, Hiroyuki Ogata

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Ecological Structuring of Temperate Bacteriophages in the Inflammatory Bowel Disease-Affected Gut Hiroki Nishiyama, Hisashi Endo, Romain Blanc-Mathieu, Hiroyuki Ogata Ecological Structuring of Temperate Bacteriophages in the Inflammatory Bowel Disease-Affected Gut Hiroki Nishiyama, Hisashi Endo, Romain Blanc-Mathieu, Hiroyuki Ogata To cite this version: Hiroki Nishiyama, Hisashi Endo, Romain Blanc-Mathieu, Hiroyuki Ogata. Ecological Structuring of Temperate Bacteriophages in the Inflammatory Bowel Disease-Affected Gut. Microorganisms, MDPI, 2020, 8 (11), pp.1663. 10.3390/microorganisms8111663. hal-03078511 HAL Id: hal-03078511 https://hal.archives-ouvertes.fr/hal-03078511 Submitted on 16 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License microorganisms Article Ecological Structuring of Temperate Bacteriophages in the Inflammatory Bowel Disease-Affected Gut Hiroki Nishiyama 1 , Hisashi Endo 1 , Romain Blanc-Mathieu 2 and Hiroyuki Ogata 1,* 1 Bioinformatics Center, Institute for Chemical Research, Kyoto University, Uji 611-0011, Japan; [email protected] (H.N.); [email protected] (H.E.) 2 Laboratoire de Physiologie Cellulaire & Végétale, CEA, CNRS, INRA, IRIG, Université Grenoble Alpes, 38000 Grenoble, France; [email protected] * Correspondence: [email protected]; Tel.: +81-774-38-3270 Received: 30 September 2020; Accepted: 23 October 2020; Published: 27 October 2020 Abstract: The aim of this study was to elucidate the ecological structure of the human gut temperate bacteriophage community and its role in inflammatory bowel disease (IBD). Temperate bacteriophages make up a large proportion of the human gut microbiota and are likely to play a role in IBD pathogenesis. However, many of these bacteriophages await characterization in reference databases. Therefore, we conducted a large-scale reconstruction of temperate bacteriophage and bacterial genomes from the whole-metagenome sequence data generated by the IBD Multi’omics Database project. By associating phages with their hosts via genome comparisons, we found that temperate bacteriophages infect a phylogenetically wide range of bacteria. The majority of variance in bacteriophage community composition was explained by variation among individuals, but differences in the abundance of temperate bacteriophages were identified between IBD and non-IBD patients. Of note, in active ulcerative colitis patients, temperate bacteriophages infecting Bacteroides uniformis and Bacteroides thetaiotaomicron—two species experimentally proven to be beneficial to gut homeostasis—were over-represented, whereas their hosts were under-represented in comparison with non-IBD patients. Supporting the mounting evidence that gut viral community plays a vital role in IBD, our results show potential association between temperate bacteriophages and IBD pathogenesis. Keywords: temperate bacteriophage; inflammatory bowel disease; ulcerative colitis; Crohn’s disease; gut microbiota 1. Introduction Inflammatory bowel disease (IBD) encompasses a group of intestinal disorders, the most common of which are Crohn’s disease (CD) and ulcerative colitis (UC). These disorders are characterized by chronic inflammation that occurs throughout multiple layers of the gastrointestinal tract in CD and in the inner layer of the colon in UC. The exact cause of IBD is not clear; however, the gut microbiota, together with host genetics and environmental factors (e.g., diet, antibiotics, and drugs), plays an important role in the pathogenesis of IBD [1,2]. Although bacteria have been the focus of most IBD-related gut microbiota studies, recent studies have shown that bacteriophages in the gut may also play an important role in the pathogenesis of IBD [3–5]. The human gut bacteriophage community is thought to be largely composed of temperate bacteriophages [6], which are characterized by their ability to replicate through two different life cycles: the lysogenic cycle and the lytic cycle [7]. In the lysogenic cycle, temperate bacteriophages are integrated into their host genome in the form of prophages. During this process, viral genes, including those associated with anti-microbial activity, virulence, and toxin production, are horizontally transferred to the host. Upon induction, temperate bacteriophages enter the lytic cycle, in which Microorganisms 2020, 8, 1663; doi:10.3390/microorganisms8111663 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 1663 2 of 15 virions are produced from prophages and released into the outer environment following lysis of the host bacterium. Recent studies on gut bacteriophage communities in IBD-affected individuals suggest that Caudovirales are associated with the pathogenesis of IBD [3,4]. However, insights based on viral taxonomy require careful consideration because the majority of viruses in the human gut are yet to be taxonomically classified [8]. Furthermore, viral taxonomy is under constant review by the International Committee on the Taxonomy of Viruses (ICTV) to accommodate newly sequenced viral genomes [9]. For example, the definition of the Caudovirales order was recently changed to include two new families: Ackermannviridae and Herelleviridae [6]. To address these problems, we aimed to characterize the ecological structure of functional temperate bacteriophage communities in the guts of IBD patients by identifying associations between these viruses and their bacterial hosts via reference-independent methods using a large publicly available microbiome dataset. 2. Materials and Methods 2.1. IBDMDB Data Depository This study was conducted using publicly available whole-metagenome shotgun sequencing (WMGS) data generated by the IBD Multi’omics Database (IBDMDB) research team as part of the Human Microbiome Project 2 [1,10]. Specifically, 1338 sets of quality-filtered WMGS data were used. Sequences (i.e., reads) were generated via DNA sequencing using the Illumina HiSeq (2 101 bp) × system (Illumina, San Diego, CA, USA) from longitudinal stool samples from 65 CD patients, 38 UC patients, and 27 non-IBD patients. Non-IBD patients had gastrointestinal symptoms but were not diagnosed with IBD [1]. Quality control of WMGS data was performed by the IBDMDB research team [1]. Briefly, the AnADAMA2 pipeline (http://huttenhower.sph.harvard.edu/anadama2) was used to remove low quality regions from reads, and any reads matching the human genome were discarded. All sequence data, including the WMGS metadata, were downloaded from the IBDMDB data depository (http://ibdmdb.org). 2.2. Assessment of Disease Activity Among CD and UC Patients CD patients with a Harvey–Bradshaw index (HBI) score 5 were identified as having active ≥ CD [11]. CD patients with an HBI score <5 were classified as having inactive CD. Among UC patients, those with a simple clinical colitis activity index (SCCAI) score 5 were identified as having active ≥ UC [12], whereas those with a SCCAI score <5 were identified as having inactive UC. 2.3. De Novo Contig Assembly Quality-filtered WMGS data from the 1327 stool samples with sufficient sequencing depth (i.e., minimum of 10,000 reads) were selected for de novo assembly. Reads from each stool sample were assembled into contiguous sequences (i.e., contigs) using MEGAHIT (version 1.1.4) (–kmin 21, –kmax 251, –k-step 10) [13]. To assemble the genomes from the microbes present at low abundance, we also co-assembled the reads from the stool samples taken from the same individual using the same method. 2.4. Generation of Viral Operational Taxonomic Units (OTUs) for Temperate Bacteriophages Viral regions within contigs were predicted using VirSorter (version 1.0.5) (–db 2, –diamond) [14]. To reduce false identification, predicted viral regions with at least one hallmark viral gene and/or enrichment of either viral-like genes or non-Caudovirales viral genes (i.e., VirSorter categories 1, 2, 4, and 5) were selected for further analyses. The selected viral regions were grouped into viral OTUs at 95% sequence similarity using CD-HIT-EST (version 4.6.8) (-c 0.95, -aS 0.85, -n 10, -g 1) [15]. To identify viral OTUs representing temperate bacteriophages, MetaGeneMark (version 4.30) was first used to derive translated peptide sequences from the viral regions [16]. Subsequently, the peptide sequences were searched against the Pfam-A database (version 33.0) using hmmscan (version 3.3) (–cut_ga) [17,18]. Viral OTUs encoding one or more of the following viral integrase protein domains were defined Microorganisms 2020, 8, 1663 3 of 15 as temperate bacteriophage and were selected for the subsequent analyses: PF00589, PF02899, PF09003, PF14659, PF13356, PF13495, PF12834, PF12835, PF13009, PF14657, PF02914, PF02316, PF02920, PF09299. Taxonomic classification of the viral OTUs was performed by classifying representative sequences (the longest) from each OTU using vConTACT v2.0 (version 0.9.12) (–rel-mode Diamond, –db ProkaryoticViralRefSeq94-Merged) [19]. 2.5. Reconstruction of Bacterial Genomes via Metagenomic Binning Contigs were binned into metagenome-assembled genomes (MAGs) using METAWRAP (version 1.1.8) (binning, –metabat2, –maxbin2, –concoct) [20]. Briefly, reads from the same
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