DNA Viral Diversity, Abundance, and Functional Potential Vary across Grassland Soils with a Range of Historical Moisture Regimes

Wu, Ruonan; Davison, Michelle; Nelson, Karen E.; Graham, Emily B.; Fansler, Sarah; Farris, Yuliya; Bell, Sheryl; Godinez, Iobani; McDermott, Jason; Hofmockel, Kirsten; Jansson, Janet

doi:10.1128/mbio.02595-21

Cited by 43 publications

(60 citation statements)

References 89 publications

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“…Soil microorganisms play key roles in these biogeochemical processes 9, 10 , and, by infecting soil microbiota 11 , viruses likely have substantial direct and indirect impacts on the resulting carbon dynamics 12 . More generally, the potential importance of viruses in soils 1, 2, 13, 14 , together with their measured high abundance (10 7 to 10 10 virus-like particles per gram of soil 1 ) and improvements in our ability to sequence and track soil viral genomes 12, 15 , has led to a renewed flurry of investigations into soil viral diversity and ecology 3–5, 16–21 . Yet, despite a new appreciation for the vast diversity of soil viruses 3–5, 16–18 , little is known about the factors that govern soil viral community assembly.…”

Section: Main Textmentioning

confidence: 99%

Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands

Santos‐Medellín

Estera-Molina

Yuan

et al. 2022

Preprint

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Although soil viral abundance, diversity, and potential roles in microbial community dynamics and biogeochemical cycling are beginning to be appreciated, little is known about the patterns and drivers of soil viral community composition that underlie their contributions to terrestrial ecology. Here, we analyzed 43 soil viromes from a precipitation manipulation experiment in a Mediterranean grassland in California, USA. We recovered 5,315 viral population sequences (vOTUs), and viral community composition exhibited a highly significant distance-decay relationship within the 18 m long field. This pattern was recapitulated in the microheterogeneity of 130 prevalent vOTUs (detected in >=90% of the viromes), which tended to exhibit significant negative correlations between genomic similarity of their predominant allelic variants and distance. Although spatial turnover was also observed in the bacterial and archaeal communities from the same soils, the signal was dampened relative to the viromes, suggesting differences in assembly drivers at local scales for viruses and their microbial hosts and/or differences in the temporal scales captured by viromes and total DNA. Despite the overwhelming spatial signal, vOTUs responsive to a decrease in soil moisture were significantly enriched in a predicted protein-sharing subnetwork of 326 vOTUs linked to 191 known actinobacteriophages, suggesting a genomically cohesive viral response to soil moisture evocative of environmental filtering, potentially by way of actinobacterial hosts. Overall, soil viral ecological processes appear to be highly constrained in space and tightly coupled to the heterogeneous, dynamic soil environment and thus fundamentally different from those of their well-mixed and more thoroughly studied marine counterparts.

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Section: Main Textmentioning

confidence: 99%

Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands

Santos‐Medellín

Estera-Molina

Yuan

et al. 2022

Preprint

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“…Viral contigs with genes annotated by a chitosanase HMM (pfam07335) were rst identi ed by applying a JGI viral detection pipeline 42 . For a more conservative functional assignment, the viral chitosanase sequences were further checked against annotation databases including EggNOG 43 , the carbohydrateactive enzyme database (CAZY) 44 and the functional ontology assignments for metagenomes database (FOAM) 45 using hmmsearch (Hmmer v3.1b2) 46 as described previously 1 and searching for sequence similarities to NCBI chitosanases using blastp 47 . The putative viral chitosanases were then screened against a pro le of lysozyme HMMs to remove the mis-annotated lysozymes (PF13702, PF00959, PF04965, PF18013, PF00062 and a self-curated lysozyme HMM 1 using the lysozyme sequences deposited at NCBI viruses (accessed on 16 November 2020).…”

Section: Methodsmentioning

confidence: 99%

“…Genes from viral contigs were predicted and translated using Prodigal 48 . The protein sequences were annotated by EggNOG bacterial and archaeal databases and three viral databases as previously described 1,49 , in addition to the 7185 microbial-speci c and 8773 viral-speci c HMMs implemented in checkV (v0.7.0) 50 . The chitosanase AMG candidates were classi ed into ve categories according to their gene positions on viral contigs and presence or absence of viral hallmark genes as described previously 1 .…”

Section: Methodsmentioning

confidence: 99%

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mentioning

confidence: 99%

“…One of these, a viral gene encoding a glycosyl hydrolase group 5 (GH5) enzyme, was cloned, expressed and found to represent a functional endomannanase 3 . The vast majority of predicted soil viral AMGs have been assigned potential functions solely based on their sequence similarities to annotated genes in microbial genomic databases 1,6 . This approach is however limited in its ability to determine if the AMG is actually expressed and if the protein is functional.…”

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confidence: 99%

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Structural characterization of a soil viral auxiliary metabolic gene encoding a functional chitosanase

Smith

Buchko

et al. 2022

Preprint

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Metagenomics is unearthing the previously hidden world of soil viruses1,2. Many soil viral sequences in metagenomes contain putative auxiliary metabolic genes (AMGs) that are not associated with viral replication. To date only one soil viral AMG has been expressed3 and none has a solved structure. Here, we aimed to establish that AMGs on soil viruses actually produce functional, active proteins. We focused on AMGs that potentially encode chitosanase enzymes that metabolize chitin – a common carbon polymer. Glycoside hydrolase family 75 viral chitosanase genes were identified from environmental metagenomes. Several of these were expressed and functionally screened. One expressed protein showing endo-chitosanase activity (V-Csn) was crystalized and structurally characterized at ultra-high resolution, thus representing the first structure of a soil viral AMG product. A structure for an inactive mutant with a bound substrate (chitosan oligomer) was also determined. Conserved active site residues in V-Csn resided in a cleft between two domains. These structures provided details about the active site, and together with structure models determined using AlphaFold2, facilitated understanding of substrate specificity and enzyme mechanism. These findings support the hypothesis that soil viruses contribute auxiliary functions to their hosts. Soil viral chitosanase AMG products that assist chitin decomposition may therefore play a previously unrecognized essential role in soil carbon cycling.

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Viral abundance and lysogenic fraction respond dynamically to cover-crop burn down and vary with conservation soil management practices

McDearis,

Zhuang,

Liang

et al. 2024

Agriculture, Ecosystems & Environment

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DNA Viral Diversity, Abundance, and Functional Potential Vary across Grassland Soils with a Range of Historical Moisture Regimes

Cited by 43 publications

References 89 publications

Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands

Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands

Structural characterization of a soil viral auxiliary metabolic gene encoding a functional chitosanase

Viral abundance and lysogenic fraction respond dynamically to cover-crop burn down and vary with conservation soil management practices

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