Bonilla-Rosso et al. 2020 - PNAS

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                <title level="a" type="main">Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota</title>
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                                <forename type="first">Germán</forename>
                                <surname>Bonilla-Rosso</surname>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                                <orgName type="department">Department of Fundamental Microbiology</orgName>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                                <forename type="first">Théodora</forename>
                                <surname>Steiner</surname>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                                <forename type="first">Fabienne</forename>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                                <forename type="first">Evan</forename>
                                <surname>Bexkens</surname>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                                <forename type="first">Philipp</forename>
                                <surname>Engel</surname>
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                                    <label>a</label> Department of Fundamental Microbiology, University of Lausanne, 1015 Lausanne, Switzerland
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                        <title level="a" type="main">Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota</title>
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                    <note type="submission">Edited by Nancy A. Moran, The University of Texas at Austin, Austin, TX, and approved February 21, 2020 (received for review January 8, 2020)</note>
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                    <p>The honey bee gut microbiota influences bee health and has become an important model to study the ecology and evolution of microbiota-host interactions. Yet, little is known about the phage community associated with the bee gut, despite its potential to modulate bacterial diversity or to govern important symbiotic functions. Here we analyzed two metagenomes derived from virus-like particles, analyzed the prevalence of the identified phages across 73 bacterial metagenomes from individual bees, and tested the host range of isolated phages. Our results show that the honey bee gut virome is composed of at least 118 distinct clusters corresponding to both temperate and lytic phages and representing novel genera with a large repertoire of unknown gene functions. We find that the phage community is prevalent in honey bees across space and time and targets the core members of the bee gut microbiota. The large number and high genetic diversity of the viral clusters seems to mirror the high extent of strain-level diversity in the bee gut microbiota. We isolated eight lytic phages that target the core microbiota member Bifidobacterium asteroides, but that exhibited different host ranges at the strain level, resulting in a nested interaction network of coexisting phages and bacterial strains. Collectively, our results show that the honey bee gut virome consists of a complex and diverse phage community that likely plays an important role in regulating strain-level diversity in the bee gut and that holds promise as an experimental model to study bacteria-phage dynamics in natural microbial communities.</p>
                    <p>honey bee | phage | microbiome | Bifidobacterium | metagenomics</p>
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                <p>The honey bee gut microbiota influences bee health and has become an important model to study the ecology and evolution of microbiota-host interactions. Yet, little is known about the phage community associated with the bee gut, despite its potential to modulate bacterial diversity or to govern important symbiotic functions. Here we analyzed two metagenomes derived from virus-like particles, analyzed the prevalence of the identified phages across 73 bacterial metagenomes from individual bees, and tested the host range of isolated phages. Our results show that the honey bee gut virome is composed of at least 118 distinct clusters corresponding to both temperate and lytic phages and representing novel genera with a large repertoire of unknown gene functions. We find that the phage community is prevalent in honey bees across space and time and targets the core members of the bee gut microbiota. The large number and high genetic diversity of the viral clusters seems to mirror the high extent of strain-level diversity in the bee gut microbiota. We isolated eight lytic phages that target the core microbiota member Bifidobacterium asteroides, but that exhibited different host ranges at the strain level, resulting in a nested interaction network of coexisting phages and bacterial strains. Collectively, our results show that the honey bee gut virome consists of a complex and diverse phage community that likely plays an important role in regulating strain-level diversity in the bee gut and that holds promise as an experimental model to study bacteria-phage dynamics in natural microbial communities.</p>
                <p>honey bee | phage | microbiome | Bifidobacterium | metagenomics B acteriophages are the top predators of the bacterial world.</p>
                <p>Due to their sheer diversity and abundance, they are considered to play central roles in the evolution, ecology, and functioning of microbial communities. Bacteriophages (phages hereafter) can modulate the composition of microbial communities and maintain high levels of diversity through kill-the-winner dynamics 
                    <ref type="bibr" target="#b0">(1)</ref>
                    <ref type="bibr" target="#b1">(2)</ref>
                    <ref type="bibr" target="#b2">(3)</ref>. They exert strong selective pressure on their hosts, accelerating their evolutionary rates and enhancing bacterial adaptability and diversification 
                    <ref type="bibr" target="#b3">(4)</ref>
                    <ref type="bibr" target="#b4">(5)</ref>
                    <ref type="bibr" target="#b5">(6)</ref>
                    <ref type="bibr" target="#b6">(7)</ref>
                    <ref type="bibr" target="#b7">(8)</ref>
                    <ref type="bibr" target="#b8">(9)</ref>
                    <ref type="bibr" target="#b9">(10)</ref>. Phage infections can increase bacterial fitness by either providing resistance to other phages 
                    <ref type="bibr" target="#b10">(11)</ref>
                    <ref type="bibr" target="#b11">(12)</ref>
                    <ref type="bibr" target="#b12">(13)</ref>, conferring competitive advantages against related strains 
                    <ref type="bibr" target="#b13">(14)</ref>
                    <ref type="bibr" target="#b14">(15)</ref>
                    <ref type="bibr" target="#b15">(16)</ref>, or mediating the horizontal transfer of beneficial functions 
                    <ref type="bibr" target="#b16">(17)</ref>
                    <ref type="bibr" target="#b17">(18)</ref>
                    <ref type="bibr" target="#b18">(19)</ref>
                    <ref type="bibr" target="#b19">(20)</ref>. Besides their importance for understanding microbial community dynamics, phage-host interactions also hold promise for applied fields of microbiology, such as bacterial phylotyping, phage therapy, and the design of engineered microbial communities 
                    <ref type="bibr" target="#b20">(21)</ref>
                    <ref type="bibr" target="#b21">(22)</ref>
                    <ref type="bibr" target="#b22">(23)</ref>.
                </p>
                <p>Recent culture-independent approaches, specifically deep sequencing of viral-like particles from various environments, have allowed us to appreciate the richness and complexity of phages in nature 
                    <ref type="bibr" target="#b19">(20,</ref>
                    <ref type="bibr" target="#b23">24)</ref>. In particular, studies on the human gut ecosystem have provided important insights about host-associated phage communities, highlighting their immense diversity and potential role for host health and disease 
                    <ref type="bibr" target="#b24">(25)</ref>
                    <ref type="bibr" target="#b25">(26)</ref>
                    <ref type="bibr" target="#b26">(27)</ref>
                    <ref type="bibr" target="#b27">(28)</ref>. Yet, the ecology and impact of phages on microbial populations are poorly understood. This is in part because many natural microbial communities are not experimentally amenable. Moreover, established experimental models often focus on single bacteria-phage pairs, whereas interactions in nature are much more complex, considering the high genetic diversity found in bacterial and phage populations 
                    <ref type="bibr" target="#b28">(29)</ref>
                    <ref type="bibr" target="#b29">(30)</ref>
                    <ref type="bibr" target="#b30">(31)</ref>
                    <ref type="bibr" target="#b19">20)</ref>. Therefore, experimental systems to study multistrain multiphage interactions are needed to expand our understanding of the ecology and impact of phages under natural settings 
                    <ref type="bibr" target="#b24">(25,</ref>
                    <ref type="bibr" target="#b31">32,</ref>
                    <ref type="bibr" target="#b20">21)</ref>.
                </p>
                <p>Honey bees harbor simple, yet highly specialized microbial communities in their guts. The bee gut microbiota is comprised of only 8 to 10 bacterial phylotypes (i.e., 16S rRNA sequences that cluster at &gt;97%), most of which contain several divergent lineages and a high extent of strain-level diversity 
                    <ref type="bibr" target="#b32">(33)</ref>
                    <ref type="bibr" target="#b33">(34)</ref>
                    <ref type="bibr" target="#b34">(35)</ref>. All bacterial phylotypes can be cultured in the laboratory and microbiotadepleted bees can be colonized with defined communities of cultured strains 
                    <ref type="bibr" target="#b35">(36)</ref>
                    <ref type="bibr" target="#b36">(37)</ref>
                    <ref type="bibr" target="#b37">(38)</ref>
                    <ref type="bibr" target="#b38">(39)</ref>. This allows us to disentangle roles of individual community members which contributes to our fundamental understanding of how microbiomes function. Moreover, recent studies have shown that the bee gut microbiota impacts the host in multiple ways 
                    <ref type="bibr" target="#b39">(40)</ref>
                    <ref type="bibr" target="#b40">(41)</ref>
                    <ref type="bibr" target="#b41">(42)</ref>. Therefore, the honey bee gut microbiota has become an important experimental model to study the ecology and evolution of microbiota-host interactions 
                    <ref type="bibr" target="#b37">(38)</ref> as well as the impact of gut bacteria on the health of this important pollinator insect 
                    <ref type="bibr" target="#b35">(36)</ref>.
                </p>
                <p>The only studies regarding honey bee-associated phages are those from the pathogens Paenibacillus larvae 
                    <ref type="bibr" target="#b42">(43)</ref>
                    <ref type="bibr" target="#b43">(44)</ref>
                    <ref type="bibr" target="#b44">(45)</ref> and Brevibacillus laterosporus 
                    <ref type="bibr" target="#b45">(46,</ref>
                    <ref type="bibr" target="#b46">47)</ref>. Phages associated with the specialized gut microbiota of honey bees have not been studied to date. We hypothesize that phages are likely to play an important Significance While bacteriophages are known to play important roles in bacterial communities, phages associated with the specialized gut microbiota of honey bees have not been characterized. We show that a diverse community of phages inhabits the bee gut targeting core bacteria of the microbiota and belonging to new viral genera with a large repertoire of unknown functions. We isolated phages infecting Bifidobacterium asteroides, a core member of the bee gut microbiota. These phages exhibited vastly different host ranges at the strain level providing insights about how diverse phage-bacteria communities coexist in nature. Our work highlights that phages play important roles in the bee gut microbiota by modulating bacterial diversity at the strain level with potential impact on bee health. role in modulating the bacterial community in the bee gut, in particular in light of the high extent of strain-level diversity that has been detected among the dominant community members of the bee gut microbiota 
                    <ref type="bibr" target="#b34">(35,</ref>
                    <ref type="bibr" target="#b47">(48)</ref>
                    <ref type="bibr" target="#b48">(49)</ref>
                    <ref type="bibr" target="#b49">(50)</ref>
                    <ref type="bibr" target="#b50">(51)</ref>
                    <ref type="bibr" target="#b51">(52)</ref>. Here, we sequenced two metagenomes (i.e., pools from ∼100 individual bee guts each), enriched for viral-like particles to characterize the phage community of the honey bee gut. We monitored the stability of the identified phage community over space and time in 73 bacterial metagenomes, isolated and characterized eight of the most abundant lytic phages, and tested their host range against a large bacterial strain collection using plaque assays. Our results show that the honey bee gut virome is comprised of a diverse community of temperate and lytic phages that target dominant members of the bee gut microbiota and hence may play an important role in regulating community dynamics. We show that a single bacterial strain can be infected by several lytic phages with different host ranges, highlighting the nested structure of the phage-bacteria interaction network in this natural bacterial community.
                </p>
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                <head>Results</head>
                <p>Sequencing of Viral-Like Particles from the Honey Bee Gut Identifies Diverse Viral Clusters. Two samples of virus-like particles (VLPs) were generated from the pooled hindguts of &gt;100 adult honey bees each sampled from two hives, Grammont (GR) and Les Droites (LD), and sequenced with Illumina technology. Reads passing a postsequencing contamination screen (98% and 99% of the reads for LD and GR, respectively) were de novo assembled, resulting in 7,016 contigs of &gt;1,000 bp for GR and 4,839 for LD. Contigs with low read coverage and lengths &lt;7,500 bp were removed. Moreover, only contigs that were categorized as viral sequences at high confidence by the software VirSorter 
                    <ref type="bibr" target="#b52">(53)</ref>, and that had a homogeneous coverage over the entire contig length (SI Appendix, Supplementary Materials and Methods), were kept for downstream analyses. These putative viral contigs identified in the two metagenomes were pooled together and redundant contigs removed. The final dataset consisted of 198 high-quality, nonidentical, representative viral contigs (SI Appendix, 
                    <ref type="figure">Fig. S1</ref>).
                </p>
                <p>We next clustered the viral contigs by gene content and protein similarity, together with sequences from the viral RefSeq database using vConTACT v2.0 
                    <ref type="bibr" target="#b53">(54,</ref>
                    <ref type="bibr" target="#b54">55)</ref> in order to assign them to viral genera and operational taxonomic units (vOTUs). As VLPs often correspond to temperate phages that can integrate into bacterial host genomes, we also included 305 prophage regions in the clustering analysis, identified in 278 bee gut-associated bacterial genomes (Dataset S1). The resulting similarity network consisted of 2,745 nodes, connected by 91,448 edges, each node corresponding to a contig from either a VLP metagenome, a viral reference sequence, or an extracted prophage region. The nodes formed 83 discrete components (i.e., subnetworks of interconnected nodes) (SI Appendix, 
                    <ref type="figure" target="#fig_2">Fig. S2</ref>).
                </p>
                <p>To focus our analysis on active phages, we mapped the raw reads from both VLP metagenomes to the sequences in the network and removed nodes corresponding to either reference sequences or contigs with less than 1× read coverage as previously suggested 
                    <ref type="bibr" target="#b55">(56)</ref>. This reduced the network to 311 nodes ( 
                    <ref type="figure">Fig. 1</ref>), 250 of which grouped into 61 clusters, and 57 of which remained unclustered, representing together 118 viral "clusters" (VCs) (Dataset S2). Eight of these VCs were not connected to the rest of the network, indicating that they are highly distinct from all other detected VCs in the two VLP metagenomes.
                </p>
                <p>To corroborate that the VCs are of viral origin and to obtain insights about their functional gene content, we looked at the annotation of 9,320 genes identified across all viral contigs. Using the Prokka bacterial and viral annotation pipeline 
                    <ref type="bibr" target="#b56">(57)</ref>, only 13% of the predicted genes had a functional annotation, i.e., 87% of the gene content represented hypothetical proteins. Many of the annotated genes coded for phage structural features or functions related to viral phage replication. However, we also identified 49 tRNA genes, most of which were associated with VC corresponding to prophages (Dataset S3). Only 70 proteincoding genes were predicted as putatively bacterial metabolic genes, distributed across 23 VCs (Dataset S3), suggesting that the identified phages carry few bacterial functions in their genomes. All except one were found in prophage contigs, and in many cases, these bacterial genes were located close to the border of the predicted prophage sequences. Therefore, we cannot exclude that these genes may also be part of the host genome, as the precise delineation of integrated prophage boundaries can be problematic 
                    <ref type="bibr" target="#b57">(58)</ref>.  
                    <ref type="figure">Fig. 1</ref>. Gene-sharing network of viral contigs identified in the two viral metagenomes generated with vConTACT v2.0 (41) and visualized using an edgeweighted spring-embedded algorithm that locates more similar contigs closer to each other. Nodes represent contigs of putative lytic (squares) or temperate (circles) phages, either from the viral metagenomes or prophage sequences that recruited reads from the metagenomic samples. Edges connect contigs that are significantly similar (darker, more significant). Shaded contours delimit contigs from the same VC. Node colors indicate the putative host according to the color legend. Abundant VCs that make up 75% of the coverage in either metagenome are labeled. Names in gray font correspond to VCs containing named phage isolates ( 
                    <ref type="figure" target="#fig_5">Fig. 4)</ref>. A list of all VCs with corresponding characteristics can be found in Dataset S2.
                </p>
                <p>To obtain further confidence about the predicted VCs, we compared all predicted proteins against the Viral RefSeq database with relaxed similarity settings (E-value &lt;1e-2 covering over 70% of the query). This approach increased the number of proteins with functional annotations from 13% to 32%. We identified sequences of viral origin in 90% of the VCs, in which an average of 26% of the genes coded for proteins involved in phage replication, virion structural proteins, phage lysins, terminases, and integrases (SI Appendix, 
                    <ref type="figure" target="#fig_3">Fig. S3</ref>), providing strong evidence that the large majority of all VCs represented phages. Proteins involved in toxin-antitoxin systems and host immunity bypass were detected in 10% of the VCs (SI Appendix, 
                    <ref type="figure" target="#fig_3">Fig. S3</ref> and Dataset S3).
                </p>
                <p>Since the probabilistic algorithm used to calculate similarity in vConTACT 
                    <ref type="bibr" target="#b53">(54)</ref> can group contigs with varying degrees of similarity, we calculated the average amino acid (AAI) and nucleotide identity (ANI) for each VC based on pairwise comparisons between contigs (SI Appendix, 
                    <ref type="figure" target="#fig_5">Fig. S4</ref>). The median AAI across all VCs was 87%, and all VCs had an AAI above 40%, suggesting that contigs within a given VC belong to the same genus according to the cutoff defined by Lavigne et al. (59) (i.e., 40% AAI). The median ANI across all VCs was 93% (with a median contig length coverage of 73%), which is below the proposed cutoff to define vOTUs (i.e., 95% ANI) 
                    <ref type="bibr" target="#b59">(60)</ref>. Only 14 VCs had ANI values above this threshold, which means that the majority of VCs contained more than one vOTU. Collectively, this indicates a high extent of genetic diversity in the phage community of the honey bee gut.
                </p>
                <p>To assign the identified VCs to taxonomic groups, we compared them to viruses in the reference database. Only 11 VCs (9%) contained sequences from the viral reference database, suggesting that they belong to previously described genera. Seventeen additional VCs could be categorized at a higher taxonomic rank using distantly related reference genomes. These 28 classified VCs (24%) belonged to the three major families within the order Caudovirales (Podoviridae, Siphoviridae, and Myoviridae), with the largest fraction representing podoviruses from the subfamily Picovirinae ( 
                    <ref type="figure" target="#fig_2">Fig. 2A</ref>). However, 91% of the detected VCs seem to belong to uncharacterized genera, and 86% could not be unambiguously classified at the family level, substantially expanding the unclassified viral sequence space.
                </p>
                <p>Taken together, our analysis shows the existence of an active VLP-producing phage community in the honey bee gut that consists of at least 118 VCs, many of which are genetically highly diverse, correspond to novel viral genera, and encode a large proportion of unknown genes.</p>
            </div>
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                <head>The Viral Community Includes Lytic and Temperate Phages that Target</head>
                <p>Major Community Members of the Honey Bee Gut Microbiota. To better understand the ecology of the identified phages, we next analyzed their lifestyle, bacterial targets, and abundance in the community. We predicted 62 VCs (52%, 
                    <ref type="figure" target="#fig_2">Fig. 2B</ref>) to represent temperate phages, as they included contigs encoding integrase genes and/or prophages present in bacterial reference genomes (Dataset S1). The remaining 56 VCs were considered to be putative lytic phages ( 
                    <ref type="figure" target="#fig_2">Fig. 2B</ref>) due to the absence of genes indicative of genomic integration. The VCs of temperate phages were strongly interconnected in our network, while most of the VCs of putative lytic phages were less connected and often formed distinct components ( 
                    <ref type="figure">Fig. 1</ref> and SI Appendix, 
                    <ref type="figure" target="#fig_2">Fig. S2</ref>). This is consistent with previous studies and suggests a higher rate of gene exchange between temperate than lytic phages 
                    <ref type="bibr" target="#b53">(54,</ref>
                    <ref type="bibr" target="#b54">55,</ref>
                    <ref type="bibr" target="#b60">61)</ref>.
                </p>
                <p>We next assigned putative hosts from the bee gut microbiota to VCs, if the latter contained contigs that had a match to CRISPR spacers or included prophages identified in the bacterial genome database (Dataset S4). This allowed us to assign 73% of the VCs to a respective bacterial host. Most of the assigned VCs were predicted to infect one of seven predominant community members of the bee gut microbiota, with the most frequent targets being Bifidobacterium (25% of the total VCs), Gilliamella (19%), Lactobacillus Firm5 (10%), and Bartonella (9%) 
                    <ref type="figure" target="#fig_2">(Fig. 2C)</ref>.
                </p>
                <p>In order to assess the relative abundance of the VCs in the two VLP metagenomes, we mapped the raw reads to the final set of viral contigs and calculated the coverage. This revealed that &gt;50% of the reads in the two VLP metagenomes came from VCs that could be taxonomically classified, with slight differences in the relative abundance of the predominant viral orders ( 
                    <ref type="figure" target="#fig_2">Fig. 2A)</ref>. Moreover, about 90% of all reads mapped to VCs of lytic phages, which shows that despite finding an equal number of VCs from temperate and lytic phages, the majority of VLPs correspond to lytic phages ( 
                    <ref type="figure" target="#fig_2">Fig. 2B</ref>).
                </p>
                <p>We next looked at the relative abundance of individual VCs across the two VLP metagenomes. Despite the difference in sequencing depth, the two metagenomes shared 99 VCs, with 113 of the total 118 VCs found in GR and 102 in LD. The viromes were dominated by 20 VCs, with 6 and 17 VCs accounting for 75% of the mapped bases from GR and LD, respectively  ( 
                    <ref type="figure" target="#fig_2">Fig. 2D</ref>). Two of these abundant VCs corresponded to temperate phages targeting Gilliamella. The remaining 18 VCs corresponded to putative lytic phages, including eight targeting Bifidobacterium, two targeting Bartonella, one targeting Lactobacillus Firm5, and seven targeting unknown hosts 
                    <ref type="figure" target="#fig_2">(Fig. 2D</ref>). This pattern is similar to that observed in other microbial communities, with a few dominant phages and a long tail of less abundant ones 
                    <ref type="bibr" target="#b61">(62)</ref>.
                </p>
                <p>Taken together, these findings show that the active viral community of the bee gut is composed of both temperate and lytic phages that target the dominant bacterial members of the bee gut microbiota.</p>
                <p>The Viral Community Is Persistent over Space and Time. To determine the prevalence of the observed viral community across bees and colonies, we analyzed 53 bacterial metagenomes that were obtained from individual bees of different ages, sampled from the same apiary as the two viral metagenomes, but in two different years 
                    <ref type="bibr" target="#b34">(35)</ref>. Even though the DNA extraction used on these samples was optimized to enrich bacterial cells rather than VLPs, all but five VCs (i.e., 113 of 118 VCs, 96%) recruited reads from at least 1 of the 53 bacterial metagenomes 
                    <ref type="figure" target="#fig_3">(Fig. 3)</ref>. The VCs had an average incidence (i.e., the percentage of samples where they were detected) of 55%, with a large difference between temperate (83%) and lytic phages (31%).
                </p>
                <p>Individual bees had a median of 77 VCs, of which 27 (35%) were lytic and 50 (65%) were temperate phages. The 20 predominant VCs were all detected across the bacterial metagenomes, indicating that they are widespread among individual bees. Significant differences in phage community composition were detected between bees of different ages (R 2 = 0.083, P = 0.003) and from different hives (R 2 = 0.081, P = 0.0002), but not across different years (R 2 = 0.01, P = 0.601), indicating that changes in the phage community may go along with changes in gut microbiota composition across colonies or seasons 
                    <ref type="bibr" target="#b34">(35,</ref>
                    <ref type="bibr" target="#b62">63)</ref> (SI Appendix, 
                    <ref type="figure">Fig. S5</ref>).
                </p>
                <p>To assess whether the identified VCs are globally distributed, we also screened a set of 20 bacterial metagenomes from two locations in Japan 
                    <ref type="bibr" target="#b63">(64)</ref>. Beta diversity analyses confirmed significant differences in VC incidence between the two countries (R 2 = 0.32, P &lt; &lt; 0.001) and between hives from the same country (R 2 = 0.37, P = 0.011) (SI Appendix, 
                    <ref type="figure">Fig. S5</ref>). Despite the geographical distance, 63% of the VCs were detected in at least one of the Japanese samples ( 
                    <ref type="figure" target="#fig_3">Fig. 3)</ref>, including phages targeting core community members of the honey bee gut microbiota.
                </p>
                <p>However, few lytic phages were found to be conserved, and of the 20 most abundant VCs, only seven were detected in the Japanese metagenomes.</p>
                <p>We conclude that despite the bias of bacterial metagenomes against lytic phages, the composition of the VLP-producing phage community in the honey bee gut microbiota is stable across time and space, but its structure and the identity of the dominant phages is variable.</p>
            </div>
            <div
                xmlns="http://www.tei-c.org/ns/1.0">
                <head>Isolation and Characterization of VLPs Infecting the Core Microbiota</head>
                <p>Member Bifidobacterium asteroides. To isolate and characterize VLPs from the honey bee gut, we prepared fresh viral filtrates from pooled honey bee guts and carried out spot tests against a total of 112 bacterial strains from our culture collection. These strains were selected among the most prevalent genera of the honey bee gut microbiota and included Lactobacilli (n = 47), Gilliamella (n = 30), Bifidobacterium (n = 20), and Frischella (n = 15). We obtained visible clearance zones for 64% of the Bifidobacterium, 50% of the Gilliamella, and 45% of the Lactobacillus strains (Dataset S5). However, only 11 lysates of strains of Bifidobacterium asteroides produced visible plaques when diluted, an indication that the lysis was caused by phages. We successfully amplified, propagated, and sequenced 10 of these 11 putative phage isolates, resulting in the reconstruction of 14 individual phage genomes ( 
                    <ref type="figure" target="#fig_5">Fig. 4A</ref> and SI Appendix, 
                    <ref type="figure">Fig. S6</ref>). Eight phage lysates appeared to be pure cultures of single phage genotypes, while from the other two preparations we were able to assemble several distinct phage genomes. The 14 genomes belonged to four distinct groups based on pairwise ANI 
                    <ref type="figure" target="#fig_5">(Fig. 4B</ref>). None of them had close matches in the viral RefSeq database, neither at nucleotide nor at protein level. However, 12 genomes clustered with viral contigs belonging to the 20 most dominant VCs identified in the two VLP metagenomes 
                    <ref type="figure">(Fig. 1)</ref>, and for all 14 genomes we had predicted the correct host based on the CRISPR spacer analysis.
                </p>
                <p>Nine of the genomes (1 through 9 in 
                    <ref type="figure" target="#fig_5">Fig. 4A</ref>) corresponded to three different vOTUs within cluster VC_52 ( 
                    <ref type="figure" target="#fig_5">Figs. 1 and 4B)</ref>, and for two of these vOTUs, we obtained four pure isolates (genomes 3, 4, 6, and 9). We thus refer to these two vOTUs as Bifidobacterium phage BadAztec and BadAargau. Both belong to the family Podoviridae, have small genomes of ∼18 kb ( 
                    <ref type="figure" target="#fig_5">Fig. 4C</ref> and SI Appendix, 
                    <ref type="figure">Fig. S6</ref>) with closest matches to Actinomyces phage Av-1 (Podoviridae:Picovirinae), and appear to belong to a large and highly diverse population of closely related viral species that are abundant in the bee gut ( 
                    <ref type="figure" target="#fig_2">Figs. 1, 2D, and 3</ref>). Two genomes (10 and 11 in 
                    <ref type="figure" target="#fig_5">Fig. 4A</ref>) corresponded to a temperate phage from the family Siphoviridae. One of them was obtained from a pure isolate (10 in 
                    <ref type="figure" target="#fig_5">Fig. 4</ref> A and C). They clustered in VC_295 and had a genome of ∼40 kb (Figs. 1 and 4B and SI Appendix, 
                    <ref type="figure">Fig. S6</ref>). We refer to them as Bifidobacterium phage BigBern. The closest hits in the viral RefSeq were Mycobacterium phage Gaia and Propionibacterium phage P100D. BigBern is the only phage isolate that belongs to a cluster that is not among the most abundant VCs in the two viral metagenomes, but it was detected in 100% of the bacterial metagenomes.
                </p>
                <p>Another phage genome (12 in 
                    <ref type="figure" target="#fig_5">Fig. 4A</ref>) that was obtained from a pure isolate clustered in VC_78, which we named BitterVaud 
                    <ref type="figure" target="#fig_5">(Figs. 1 and 4A)</ref>. This phage had a much larger genome than the other isolates (51.7 kbp, SI Appendix, 
                    <ref type="figure">Fig. S6</ref>) and belonged to the family Siphoviridae ( 
                    <ref type="figure" target="#fig_5">Fig. 4 A and C)</ref>, with closest hits to Rhodococcus phage RequiPepy6 and Arthrobacter phage Mudcat. Cluster VC_78 was closely related to VC_76 in the similarity matrix ( 
                    <ref type="figure">Fig. 1</ref>). Together these two VCs represent &gt;30% of all reads in the two viral metagenomes 
                    <ref type="figure" target="#fig_2">(Fig. 2D</ref>), suggesting that the isolate of BitterVaud represents one of the most abundant phage lineages in the bee gut.
                </p>
                <p>The last two genomes (13 and 14 in 
                    <ref type="figure" target="#fig_5">Fig. 4A</ref>) were obtained from pure isolates (named BlindBasel and BraveUri) and belonged to VC_291 ( 
                    <ref type="figure" target="#fig_5">Figs. 1 and 4A</ref>). Their genomes (32 kb, SI Appendix, 
                    <ref type="figure">Fig. S6</ref>) shared 94.1% ANI over 83% of their length ( 
                    <ref type="figure" target="#fig_5">Fig. 4B)</ref>, which is at the threshold to delimit vOTUs (&gt;95% ANI over &gt;80% length), and suggests that they either represent very closely related species or two populations in the process of differentiation. Their morphology and genomes position them within Siphoviridae ( 
                    <ref type="figure" target="#fig_5">Fig. 4 A and C)</ref>, and their closest hits are to Mycobacterium phage Rumpelstiltskin, Synechococcus phage S-CBS1, and Pseudoalteromonas phage Pq0.
                </p>
                <p>In summary, we established and characterized eight pure and two mixed phage isolates, of which we obtained 14 phage genomes corresponding to four distinct VCs, all of which target the same core member of the honey bee gut microbiota, B. asteroides. These results confirm the viability and predicted host targets of some of the most abundant VCs, and demonstrate their experimental tractability. Considering the large extent of strain-level diversity in the honey bee gut microbiota, we sought to test the host range of the eight pure phage isolates against all 57 bacterial isolates of Bifidobacterium in our culture collection. A total of 26 bacterial strains displayed susceptibility to at least one of the phages 
                    <ref type="figure" target="#fig_5">(Fig. 4D</ref> and Dataset S6). All strains were insensitive to at least one phage, and 54% of the strains were insensitive to all phages. We detected 10 different susceptibility patterns among the tested bacterial strains 
                    <ref type="figure" target="#fig_5">(Fig. 4D</ref>). However, there was no evident association with the phylogenetic relatedness of the bacteria in that specific clades of  to the corresponding phage. A bacterial strain was considered susceptible when plaque formation was observed in at least three replicates and when those replicates accounted for more than 50% of the replicates. Translucent colors indicate that plaque formation was observed in a number of replicates below this threshold. The phylogeny of the host strains was inferred from a 343-bp fragment of the housekeeping gene sdhA using maximum likelihood (GAMMACAT + HKY85, alpha = 0.37). Black circles indicate bootstrap support &gt;800 of 1,000 replicates. Five publicly available genomes of B. asteroides were included into the phylogeny for reference.
                </p>
                <p>closely related bacterial strains tended to be susceptible to the same phage, or that individual phages infected closely related strains exclusively 
                    <ref type="figure" target="#fig_5">(Fig. 4D</ref>). In fact, closely related strains (even those isolated from the same hive or year) displayed very different susceptibility patterns (e.g., ESL0198 and BM3_17, 
                    <ref type="figure" target="#fig_5">Fig. 4D</ref>). Moreover, phages displayed distinct host ranges, with the podoviral isolates (BadAztec and BadAargau) showing a more narrow range than BitterVaud or BlindBasel. Interestingly, two bacteria strains (ESL199 and ESL200) were susceptible to a phage despite carrying matching CRISPR spacers, suggesting that the presence of spacers is not sufficient to predict the host range of these phages. However, as we only had four genomes of the analyzed strains available, it was not possible to carry out a more comprehensive analysis.
                </p>
                <p>In conclusion, the widespread insensitivity to infection and the varying susceptibility patterns indicate that the host range among the tested phages is determined at the strain level. Moreover, our results suggest the existence of nested higher-order interactions, involving multiple phages with overlapping host ranges and multiple strains with different phage susceptibility.</p>
            </div>
            <div
                xmlns="http://www.tei-c.org/ns/1.0">
                <head>Discussion</head>
                <p>The present study provides several important advances in our understanding of gut-associated phage communities and their specific role for the bee gut microbiota. First, we show that honey bees harbor a diverse community of temperate and lytic phages in their guts, most of which represent novel viral genera with a large repertoire of unknown gene functions. Second, we reveal that the phage community is conserved in honey bees across space and time and targets major bacterial members of the bee gut microbiota. Third, we demonstrate that the phage community is experimentally amenable, as we could propagate some of the most abundant phages in vitro and test their host range across a large number of bacterial strains. Fourth, we find that the bacterial susceptibility to phages from the bee gut largely differs at the strain level and that phages targeting the same strain can have vastly different host ranges. These findings illustrate the complexity of bacteria-phage interactions in nature and suggest that the coexistence of phages targeting the same community member may be facilitated by distinct infection strategies and ecological traits.</p>
                <p>We applied strict cutoffs for detecting metagenomic contigs as viral sequences and assigning them to VCs, because of the risk of sequencing contaminants or bacterial DNA in VLP samples of low biomass. Although a large fraction of the identified gene content represented hypothetical proteins, most of the VCs contained at least some genes with homology to known prokaryotic viral genes. Therefore, we are confident that most of the identified VCs represent phages, providing a solid basis for investigating the viral community in the honey bee gut. However, it should be noted that due to our strict cutoffs certain phages may have been missed, in particular those with small genomes or unusual coding content. Moreover, our sequencing strategy was selective for double-strand DNA, i.e., all single-strand RNA and DNA viruses, including known honey bee viruses, were excluded from our analysis.</p>
                <p>Most of the identified VCs corresponded to novel viral genera lacking close hits in the reference database. Nonetheless, based on the identification of matching CRISPR spacers and integrated prophage regions, we were able to determine that the majority (73%) of the VCs target core members of the bee gut microbiota 
                    <ref type="bibr" target="#b32">(33)</ref>
                    <ref type="bibr" target="#b33">(34)</ref>
                    <ref type="bibr" target="#b34">(35)</ref>. This is remarkable, given that the percentage of phages that can be assigned to a host in, e.g., the human gut, is consistently below 3% 
                    <ref type="bibr" target="#b26">(27,</ref>
                    <ref type="bibr" target="#b64">65,</ref>
                    <ref type="bibr" target="#b65">66)</ref>.
                </p>
                <p>Several VCs contained a high extent of genetic diversity, suggesting that they represent several vOTUs of the same genus 
                    <ref type="bibr" target="#b59">(60,</ref>
                    <ref type="bibr" target="#b66">67)</ref>. This high genetic diversity seems to stand in contrast to the few bacterial phylotypes constituting the bee gut microbiota 
                    <ref type="bibr" target="#b32">(33)</ref>. However, previous studies have shown that most phylotypes consist of several sublineages which in turn harbor a large number of divergent bacterial strains 
                    <ref type="bibr">(48-52, 35, 68)</ref>. Correspondingly, our experiments revealed that different phages target different strains of the same phylotype, illustrating that specialization occurs at the strain rather than the phylotype level. Moreover, the largest proportion of VCs with a predicted bacterial host corresponded to phages of B. asteroides, which is the phylotype with the highest genetic diversity in the bee gut microbiota 
                    <ref type="bibr" target="#b34">(35)</ref>. Therefore, the high level of genetic diversity in the viral community seems to mirror the high extent of strainlevel diversity among the bacterial phylotypes of the bee gut microbiota.
                </p>
                <p>Under the assumption that phage-bacteria interactions follow classical predator-prey dynamics (i.e., kill the winner) (1), we would expect that the phage community in the bee gut is highly variable and that the two metagenomes present only a snapshot of the existing diversity. In addition, each of the two samples corresponded to pools of &gt;100 bee guts, making it unclear if the identified phages cooccur in individual bees. However, by recruiting reads from bacterial metagenomes, sampled from the same apiary as the VLP metagenomes, to the identified VCs we show that distinct phages coexist in individual bees, and that the phage community is persistent and temporally stable. In contrast, the viral community seems to be more variable across space, because only half of the VCs, which were derived from samples from Switzerland, recruited reads from bacterial metagenomes from Japan. Temporal stability has been reported for the gut viromes of human individuals over roughly the same time scale 
                    <ref type="bibr" target="#b26">(27)</ref>, and this has previously been attributed to the dominance of phages with a temperate lifestyle 
                    <ref type="bibr" target="#b65">(66,</ref>
                    <ref type="bibr" target="#b68">69,</ref>
                    <ref type="bibr" target="#b69">70)</ref>. Temperate phages contributed a significant portion of the viral community in the bee gut and were more abundant than most of the lytic phages across the analyzed bacterial metagenomes. Collectively, these findings seem to conform with the piggyback-the-winner model, which predicts that a lysogenic lifestyle is more advantageous than a lytic one when host densities and growth rates are high 
                    <ref type="bibr" target="#b70">(71)</ref>, such as in the gut of metazoans 
                    <ref type="bibr" target="#b69">(70)</ref>. However, bacterial metagenomes are biased against VLPs, which would mean that a large proportion of the detected sequences likely comes from integrated temperate phages and not from VLPs produced by lytic replication. Moreover, when taking relative abundance into account, lytic phages dominated the two VLP metagenomes, a pattern that has been recently reported for human viromes too 
                    <ref type="bibr" target="#b26">(27)</ref>. Although it is tempting to discuss which model describes the dynamics of the phage community in the honey bee gut, this requires a dataset that quantitatively compares abundance, persistence, and fitness of both lytic phage particles and temperate integrated lysogens simultaneously. Nevertheless, our current study demonstrates that temperate phages produce active viral particles in the honey bee gut, but that they are outnumbered in abundance by lytic phages.
                </p>
                <p>Our understanding of bacteria-phage interactions in gut microbial communities is limited by the availability of experimentally tractable systems. For example, only a few studies have investigated bacteria-virus interactions in mouse models 
                    <ref type="bibr" target="#b20">(21,</ref>
                    <ref type="bibr" target="#b31">32)</ref>, and one of the most ubiquitous phages of the human gut virome has only recently been isolated 
                    <ref type="bibr" target="#b71">(72)</ref>. In the present study, we complemented our metagenomic analysis with experimental approaches to better understand interactions underlying the identified viral diversity in the bee gut. We report eight pure phage isolates that target core bacteria from the honey bee gut microbiota, including lytic phages for the genus Bifidobacterium (73). All phage isolates belonged to VCs that were highly abundant in the two viral metagenomes or ubiquitous across samples from individual bees. We thus believe that they belong to some of the most prevalent viruses in the bee gut, possibly explaining why we were able to isolate and amplify them from the viral filtrates.
                </p>
                <p>The availability of distinct phage isolates together with a large bacterial strain collection allowed us to analyze the interaction network underlying the coexistence of diverse viruses and bacterial strains in the bee gut. The analyzed phages had overlapping host ranges, but differed significantly in the number of hosts they infected. In turn, divergent host strains could be infected by the same phage, while displaying different susceptibility to the tested phages. This pattern is characteristic of a nested network, also observed in other bipartite interaction systems and reported as the common pattern in phage-bacteria interaction networks resolved at bacterial strain resolution 
                    <ref type="bibr" target="#b55">(56,</ref>
                    <ref type="bibr" target="#b56">57)</ref>.
                </p>
                <p>A theoretical model predicts that a stable coexistence can emerge in nested interaction networks if both, hosts and phages, have differential life history traits 
                    <ref type="bibr" target="#b1">(2)</ref>. Indeed, B. asteroides strains have been shown to occupy distinct metabolic niches in the bee gut (68) and carry vastly different gene content 
                    <ref type="bibr" target="#b48">(49)</ref>, while the tested phage isolates vary in their genome size, lifestyle, phylogeny, and host range. Therefore, the observed nested interaction network in combination with the distinct viral and bacterial ecology seems to be sufficient to explain the coexistence between diverse viruses and host strains in the bee gut.
                </p>
                <p>Regardless of the underlying mechanism, the coexistence of phages and their hosts across time suggests complex population dynamics that potentially affect the bacterial community structure in the bee gut. For example, recent studies have shown that individual phages can knock down bacterial hosts in artificial communities in the mouse gut with cascading effects on the relative abundance of other community members 
                    <ref type="bibr" target="#b20">(21)</ref>. In the same way, phages in the bee gut may contribute to the segregation of bacterial strains across individual honey bees, resulting in the observed individualized community profiles at the strain level 
                    <ref type="bibr" target="#b34">(35,</ref>
                    <ref type="bibr" target="#b63">64)</ref>, with important consequences for the function of the microbiota.
                </p>
                <p>Two important factors that have likely driven the diversification of the bee gut microbiota are adaptation to different metabolic niches and the segregation of bacteria among divergent host species and populations 
                    <ref type="bibr" target="#b34">(35,</ref>
                    <ref type="bibr" target="#b36">37,</ref>
                    <ref type="bibr" target="#b39">40)</ref>. However, it is known that predation plays a key role in regulating diversity in natural ecosystems in a top-down fashion 
                    <ref type="bibr" target="#b73">(74)</ref>. Therefore, it is tempting to speculate that phages may have contributed to the generation and maintenance of diversity in the honey bee gut, in particular at the strain level. This hypothesis is supported by the observation that the community member with the highest genetic diversity overall and per individual bee 
                    <ref type="bibr" target="#b34">(35)</ref>, is the one with the most diverse set of phages, i.e., B. asteroides. Divergent bacterial strains carry different metabolic functions, and high bacterial diversity has been associated with resilience to community invasion. Consequently, the interaction of phages with their bacterial hosts and their impact on the bacterial diversity may play an important role for bee health and disease.
                </p>
                <p>Future studies will profit from the tractability of the identified phages and their bacterial hosts, which together with the available gnotobiotic bee model 
                    <ref type="bibr" target="#b37">(38)</ref> will not only advance our understanding of general aspects of phage-bacteria interactions in animal hosts, but also their specific role for bee gut microbiota and bee health.
                </p>
            </div>
            <div
                xmlns="http://www.tei-c.org/ns/1.0">
                <head>Methods</head>
                <p>Detailed protocols are available in SI Appendix, Supplementary Materials and Methods. Viral Metagenomes. Bees from two hives located at the University of Lausanne were sampled in January 2017 and February 2018. VLPs were isolated from the pooled hindguts of each of the samples with a polyethylene glycol (PEG) precipitation protocol. Phage DNA was extracted and sequenced using Illumina. The reads were assembled with SPAdes (75) and high-quality, nonredundant viral contigs were selected based on the identification of viral sequences with VirSorter (53), contig length, and read coverage. Sequences of putative prophages were identified with PHASTER (76) in 291 publicly available isolate genomes of bee gut bacteria. They were clustered together with the viral metagenomic contigs according to their protein content and protein similarity using vConTACT v2.0 
                    <ref type="bibr" target="#b53">(54,</ref>
                    <ref type="bibr" target="#b54">55)</ref> resulting in a gene-sharing network of viral sequences. VCs that did not recruit viral metagenomic reads were removed from the network and the ANIs and AAIs were calculated per VC. Sequences from VCs were annotated with Prokka (57), and further functionally annotated by blasting them against the Viral RefSeq. CRISPR spacer sequences were identified in the same bacterial genome dataset used for prophage identification with CRISPRCasFinder (77), and spacer sequences were blasted against the sequences in the VCs. A putative host was assigned to a VC when it contained a contig with a hit to a CRISPR spacer or a contig from a phage with a known host. A temperate lifestyle was assigned to contigs containing integrases or prophage regions. Taxonomic ranks were assigned to a VC when it included reference contigs with known taxonomy or had blast hits against a particular order of viruses.
                </p>
                <p>Phage Isolates and Host Range. Bees from two hives were sampled in October 2017 and 2018, and VLPs were extracted. The resulting phage solutions were used to screen for phage susceptibility in a total of 112 bacterial strains from our culture collection. Positive plaques were extracted, filter sterilized, and subjected to a serial dilution test to confirm phage presence. Confirmed phage solutions were then successively purified and amplified. DNA was extracted and sequenced using Illumina, and reads were assembled with SPAdes 
                    <ref type="bibr" target="#b74">(75)</ref>. Assembled genomes were annotated with Prokka (57), and their sequences incorporated in the viral contig similarity network described above. Eight pure phage isolates were screened against 57 strains of B. asteroides from our culture collection to evaluate their host range. Host susceptibility was established when a lysis plaque was observed in at least 50% of the total replicates. Primers targeting a region of the sdhA gene from the B. asteroides were designed, and sequences were amplified and Sanger sequenced. The sdhA sequences were aligned with Clustal Omega 
                    <ref type="bibr" target="#b77">(78)</ref> and the phylogeny of B. asteroides strains was inferred using maximum likelihood in RAxML (GAMMACAT + HKY85, alpha = 0.37) (79).
                </p>
                <p>Data Availability. Sequencing data of the two viromes has been deposited under BioProject PRJNA599270. The genomes of the eight pure phage isolates have been deposited in GenBank, under accession numbers MT006233-MT006240. Custom code and intermediate data files are available in GitHub (https://github.com/geboro/HoneyBee-Virome-2020). Bacterial metagenomes from Japan are deposited under BioProject PRJNA598094, and those from Switzerland are deposited under BioProject PRJNA473901.</p>
            </div>
            <figure
                xmlns="http://www.tei-c.org/ns/1.0" xml:id="fig_2">
                <head>Fig. 2 .</head>
                <label>2</label>
                <figDesc>Characterization of the VCs identified in the two viral metagenomes. (A) Proportion of VCs per taxonomic annotation at family level. (B) Proportions of VCs predicted to have a temperate or lytic lifestyle. (C) Proportion of VCs per predicted bacterial target. "GR" and "LD" indicate the relative proportions in each viral metagenome. "Pooled" depicts the proportions across both viral metagenomes. "Unweighted" shows raw counts based on the de novo assembly, while "Weighted" shows counts normalized per base coverage and hence indicates the relative abundances in the phage samples. (D) Blue and orange boxes indicate which VCs contribute to &gt;75% of the relative abundances in each viral metagenome (six VCs for sample GR and 17 VCs for sample LD, 20 VCs in total). The relative abundance of these 20 VCs in each sample is given next to it (Upper bar for GR, Lower bar for LD). Relative abundances were calculated based on coverage per base per contig in each VC.</figDesc>
            </figure>
            <figure
                xmlns="http://www.tei-c.org/ns/1.0" xml:id="fig_3">
                <head>Fig. 3 .</head>
                <label>3</label>
                <figDesc>Distribution of the viral community across individual bees and stability over space and time. (A) Detection of VCs in 73 bacterial metagenomes of individual honey bees from Switzerland and Japan. Per-base per-contig coverage of mapped reads to VCs is depicted as a heatmap of relative abundances in log10 scale (log10 values below zero indicate coverage below 1×, and −2 indicates no reads recruited). Samples are ordered according to country (Switzerland and Japan) and colony (black and gray bars), and for the Swiss samples also according to age (Y, young, M, middle age, O, old; see ref. 32). VCs are sorted according to lifestyle (lytic vs. temperate). (B) Incidences of VCs across individual bees from Switzerland and Japan. VC order is the same in the two panels.</figDesc>
            </figure>
            <figure
                xmlns="http://www.tei-c.org/ns/1.0" xml:id="fig_4">
                <head>The</head>
                <label></label>
                <figDesc>Host Range Varies among B. asteroides Phages, Suggesting Complex Multiphage Multistrain Interactions in the Honey Bee Gut.</figDesc>
            </figure>
            <figure
                xmlns="http://www.tei-c.org/ns/1.0" xml:id="fig_5">
                <head>Fig. 4 .</head>
                <label>4</label>
                <figDesc>Lytic phages targeting B. asteroides show a wide range of host specificities. (A) Characteristics of the 14 genomes derived from 10 phage lysates. Eight genomes were obtained from pure lysates, which were used in subsequent experiments. Six genomes were obtained from mixed lysates, which were neither used for experiments nor given isolate names. The numbering of genomes/isolates of A is also used in B, C, and D. (B) ANI between the 14 genomes. Same color indicates phage genomes belonging to the same vOTU, and the ANI values are indicated for each pair unless ANI was below 70% or the overlap between genomes was less than 60%. (C) Electron micrographs of four of the eight isolated phages. Scale bars are indicated for each image. Phage identities clockwise from the Upper Left-most image: BadAztec1 (phage 3), BlindUri1 (phage 14), BitterVaud2 (phage 12), and BigBern1 (phage 10). No imaging was done for other phage isolates. (D) Host interaction results of the eight pure phage isolates targeting B. asteroides. Solid filled circles indicate strain sensitivity</figDesc>
            </figure>
            <note
                xmlns="http://www.tei-c.org/ns/1.0" place="foot" n="2">of 8 | www.pnas.org/cgi/doi/10.1073/pnas.2000228117 Bonilla-Rosso et al. Downloaded at Akademiska Sjukhuset on March 16, 2020
            </note>
            <note
                xmlns="http://www.tei-c.org/ns/1.0" place="foot" n="4">of 8 | www.pnas.org/cgi/doi/10.1073/pnas.2000228117 Bonilla-Rosso et al. Downloaded at Akademiska Sjukhuset on March 16, 2020
            </note>
            <note
                xmlns="http://www.tei-c.org/ns/1.0" place="foot" n="6">of 8 | www.pnas.org/cgi/doi/10.1073/pnas.2000228117 Bonilla-Rosso et al. Downloaded at Akademiska Sjukhuset on March 16, 2020
            </note>
            <note
                xmlns="http://www.tei-c.org/ns/1.0" place="foot">Downloaded at Akademiska Sjukhuset onMarch 16, 2020   
            </note>
        </body>
        <back>
            <div type="acknowledgement">
                <div
                    xmlns="http://www.tei-c.org/ns/1.0">
                    <p>The authors declare no competing interest.</p>
                </div>
                <div
                    xmlns="http://www.tei-c.org/ns/1.0">
                    <head>This article is a PNAS Direct Submission.</head>
                    <p>Published under the PNAS license. ACKNOWLEDGMENTS. P.E. is supported by the European Research Council ERC-StG "MicroBeeOme" (grant 714804), the Human Frontier Science Program Young Investigator grant RGY0077/2016, and the Swiss National Science Foundation project grant 31003A_179487. We thank Ryo Miyazaki and Shota Suenami for providing the Japanese metagenomes from Apis mellifera (BioProject PRJNA598094), and Kirsten Ellegaard for access to the processed data. We appreciate the assistance and support of Caroline Kizilyaprak and Jean Daraspe from the electron microscopy facility at Lausanne University. Finally, we would like to thank Alexander Harms, Marc Garcia-Garcera, Vincent Somerville, and two anonymous reviewers for contributing suggestions to improve this manuscript.</p>
                </div>
            </div>
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    </text>
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