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Viromes Outperform Total Metagenomes in Revealing the Spatiotemporal Patterns of Agricultural Soil Viral Communities

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Viromes Outperform Total Metagenomes in Revealing the Spatiotemporal Patterns of Agricultural Soil Viral Communities bioRxiv preprint doi: https://doi.org/10.1101/2020.08.06.237214; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Viromes outperform total metagenomes in revealing the spatiotemporal patterns 2 of agricultural soil viral communities 3 Christian Santos-Medellin1, Laura A. Zinke1, Anneliek M. ter Horst1, Danielle L. Gelardi2, 4 Sanjai J. Parikh2, and Joanne B. Emerson1,3 5 6 1Department of Plant Pathology, University of California, Davis, One Shields Avenue, 7 Davis, California, USA, 95616 8 2Department of Land, Air and Water Resources, University of California, Davis, One 9 Shields Avenue, Davis, California, USA, 95616 10 3Genome Center, University of California, Davis, One Shields Avenue, Davis, California, 11 USA, 95616 12 13 Corresponding author information: 14 Joanne B. Emerson 15 Address: One Shields Ave, Davis, California, USA, 95616 16 Email: [email protected] 17 Phone: 530-752-9848 18 19 Running title: “Spatiotemporal trends of soil viral communities” 20 21 Competing interests: Authors declare no conflict of interest 22 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.06.237214; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 23 Abstract 24 25 Viruses are abundant yet understudied members of soil environments that influence 26 terrestrial biogeochemical cycles. Here, we characterized the dsDNA viral diversity in 27 biochar-amended agricultural soils at the pre-planting and harvesting stages of a tomato 28 growing season via paired total metagenomes and viromes. Size fractionation prior to 29 DNA extraction reduced sources of non-viral DNA in viromes, enabling the recovery of a 30 vaster richness of viral populations (vOTUs), greater viral taxonomic diversity, broader 31 range of predicted hosts, and better access to the rare virosphere, relative to total 32 metagenomes, which tended to recover only the most persistent and abundant vOTUs. 33 Of 2,961 detected vOTUs, 2,684 were recovered exclusively from viromes, while only 34 three were recovered from total metagenomes alone. Both viral and microbial 35 communities differed significantly over time, suggesting a coupled response to 36 rhizosphere recruitment processes and nitrogen amendments. Viral communities alone 37 were also structured along a spatial gradient. Overall, our results highlight the utility of 38 soil viromics and reveal similarities between viral and microbial community dynamics 39 throughout the tomato growing season yet suggest a partial decoupling of the processes 40 driving their spatial distributions, potentially due to differences in dispersal, decay rates, 41 and/or sensitivities to soil heterogeneity. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.06.237214; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 42 Introduction 43 44 Viruses are ubiquitous and abundant members of Earth’s ecosystems that can affect the 45 assembly, dynamics, and function of microbial communities (1–3). They control the size 46 of microbial populations via infection and lysis, redirect microbial metabolism through 47 auxiliary metabolic genes (4–8), and mediate gene transfer across hosts (9,10). In soils, 48 one gram can harbor up to 1010 viruses (11,12), sometimes surpassing the number of 49 coexisting bacteria (13). Similar to their role in marine systems (3), recent studies suggest 50 that viruses may be key contributors to carbon and nutrient cycling in terrestrial 51 environments (14–16). Despite this ecological relevance, soil viral communities and the 52 factors shaping them are poorly understood (9,10,17). 53 Viral replication depends on the successful infection of suitable hosts. As such, the 54 abundances of viral populations and, consequently, the structure of viral communities are 55 inherently linked to the compositional trends of coexisting host communities (18–20). In 56 agricultural soils, rhizosphere processes can alter microbial diversity by actively 57 promoting or inhibiting the recruitment of select taxa (21,22). Soil amendments can further 58 affect microbiome structure by shifting the quantity and quality of available nutrients (23). 59 Understanding whether viral communities display similar trends is essential to unravel the 60 potential of host-virus interactions to affect microbially-influenced soil properties. 61 Additionally, environmental factors such as temperature, pH, nutrient status, and moisture 62 could directly contribute to viral community variation by differentially impacting the activity 63 and decay of soil viruses (24). Similarly, viral adsorption to soil particles could influence 64 the spatial distribution of viruses by limiting virion movement across the soil matrix (24). 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.06.237214; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 65 Thorough characterization of viral diversity patterns across a variety of soil conditions 66 could shed new light on the drivers of viral community dynamics. 67 Given the absence of a universal marker gene across viral genomes, metagenomic 68 approaches are necessary to survey viral community diversity (25). For soils, recent 69 studies have usually relied on the recovery of viral sequences from whole shotgun 70 metagenomic datasets (14,26,27). This approach not only capitalizes on the existence of 71 streamlined wet lab workflows but also facilitates the simultaneous characterization of the 72 microbial and viral fractions (10). While convenient, most sequences in these total 73 metagenomes are derived from bacterial and eukaryotic genomes (26), presumably 74 concealing the less abundant viral signal unless deep sequencing efforts are performed 75 (10). Moreover, the vast microbial richness associated with soil environments (28) 76 typically results in high-complexity sequence profiles that are challenging to assemble de 77 novo (29), further hindering the identification of viral genomes. 78 Viral communities can be also characterized by physically separating virions from 79 larger microbes through filtration prior to DNA extraction and sequencing. The resulting 80 viral size-fraction metagenomes, or viromes, have increased coverage of viral sequences 81 and can therefore capture a more complete picture of viral diversity relative to total 82 metagenomes (10,30). While this viromic approach has been successfully adopted to 83 study aquatic systems (3,31–33), it has been challenging to implement for soil 84 environments (10), mainly due to low DNA extraction yields that can preclude library 85 construction and sequencing (30). Early soil viromic studies used multiple displacement 86 amplification (MDA) and/or Random Amplified Polymorphic DNA (RAPD) PCR to bypass 87 this limitation (34), however amplification biases, particularly for MDA, preclude 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.06.237214; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 88 quantitative estimations of viral community composition using these approaches (35). 89 Until recently, large amounts of soil input were required to avoid these amplification 90 biases, but recent improvements in library construction from nanograms of DNA now 91 make it practical to work with manageable amounts of soil (~50 g or less) per sample 92 (30). Continuous development of optimized extraction workflows has enabled virome 93 preparation from a variety of soils (15,36), greatly expanding our ability to examine viral 94 diversity in these environments. 95 Here, we use a combination of total metagenomes and viromes to characterize 96 soil dsDNA viral communities associated with an agricultural tomato field. First, we 97 compare the performance of the two profiling approaches, in terms of their ability to 98 recover diverse viral sequences, and then we explore viral and microbial ecological 99 patterns in our data. We find that viromes vastly outperform total metagenomes in the 100 recovery of viral diversity and that viral communities display strong spatiotemporal 101 dynamics, which are only partially explainable by shared patterns with bacterial host 102 communities and environmental conditions. 103 104 Materials and Methods 105 106 Sample collection 107 Samples were collected from a tomato agricultural field in Davis, CA, USA (38°32’08” N, 108 121°46’22” W) within the context of a larger ongoing study of the impacts of biochar on 109 agricultural production. The soil is classified as Yolo silt loam, a fine-silty, mixed, 110
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