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Study siteThe study was carried out in post-agriculture forests at different growth stages near the forest reserve of Yoko (N00°17′; E25°18′; mean elevation 435 m a.s.l.), situated between 29 and 39 km south east of Kisangani, in the Democratic Republic of the Congo. We set up 15 (40 × 40 m) plots, set out in triplicate along five successional stages (15 plots): agriculture and 5, 12, 20, 60 years old secondary forest (respectively, 5 yrs, 12 yrs, 20 yrs, 60 yrs). Additionally, soils were also characterized in three agricultural plots (Ag). We interviewed owners, farmers, and local experts to determine the time-since-disturbance of all plots. Tree height measurements were recorded at the plot level for 20% of individuals of each diameter class. The climax vegetation in the region is classified as semi-deciduous tropical. Climate falls within the Af-type following the Köppen-Geiger classification33. Annual rainfall ranges from 1418 to 1915 mm with mean monthly temperatures varying from 23.7 to 26.2 °C. Throughout the year, the region is marked by a long and a short rainy season interrupted by two small dry seasons December–January and June–August. Soils in the region are highly weathered Oxisols, being poor in nutrients, with low pH and dominated by sandy texture.Sampling and sample analysisThroughfall and bulk precipitation was collected weekly using polyethylene (PE) funnels supported by a wooden pole of 1.5 m height to which a PE tube was attached and draining into 5 L PE container. A nylon mesh was placed in the neck of the funnel to avoid contamination by large particles. The container was buried in the soil and covered by leaves to avoid the growth of algae and to keep the samples cool. We installed eight throughfall collectors in each plot as two rows of four collectors, with approximately 8 m distance between all collectors. On every sampling occasion, the water volume in each collector was measured in the field, and recipients, funnels and mesh were replaced, rinsed with distilled water. A volume-weighted composite sample of the devices per plot was made. All samples were stored in a freezer immediately and sent in batch to Belgium for chemical analysis. The volume-weighted composite samples were first filtered using a nylon membrane filter of 0.45 µm before freezing. Total phosphorus was measured by inductively coupled plasma atomic emission spectroscopy (ICP AES, IRIS interpid II XSP, Thermo Scientific, USA). Although we acknowledge the potential for microbial activity in the collectors during a 1-week, dark, in situ storage of the samples, the use of total phosphorus concentration and lack of algal growth allow for complete phosphorus recovery.Following analysis, the samples from the replicate field sites per forest stage were pooled into ‘weekly’ forest-type samples, and these were subsequently analyzed for dissolved black carbon (DBC). In short, the pooled water samples were acidified to pH 2 and analyzed for dissolved organic carbon (DOC) concentration via high-temperature catalytic oxidation on Shimadzu TOC-L total organic carbon analyzer following established methodology34. DOC was isolated from the water samples by solid phase extraction (SPE) following Dittmar et al.35. Briefly, SPE cartridges (Varian Bond Elut PPL, 1 g, 6 mL) were conditioned sequentially with methanol, ultrapure water, and ultrapure water acidified to pH 2 using concentrated HCl, then passed through the SPE cartridges by gravity. SPE cartridges were dried under a stream of high-purity N2 gas. DOC was eluted from the SPE cartridge with methanol (SPE-DOC) and stored at −20 °C until further analysis. DBC was quantified using the benzenepolycarboxylic acid (BPCA) method as detailed in Wagner et al.20. The BPCA approach to quantifying DBC involves chemothermal oxidation of condensed aromatic DOC compounds to benzenehexacarboxylic acid (B6CA) and benzenepentacarboxylic acid (B5CA) products. The B6CA and B5CA oxidation products are robustly measured and derive exclusively from pyrogenic sources36. Condensed aromatic DBC, as measured using the BPCA method, is ubiquitous in aquatic environments globally21,37,38,39. DBC has also been quantified in throughfall and stemflow in longleaf pine forests that undergo regular prescribed burning40. Therefore, we use the BPCA method as a proxy for carbon inputs from biomass burning in the current study. To analyze our samples for BPCAs, aliquots of SPE-DOC (~0.5 mg C equivalents) were combined with concentrated HNO3 in flame-sealed glass ampoules and heated to 160 °C for 6 h. The resultant BPCA-containing residue was dried and re-dissolved in mobile phase for subsequent analysis. Individual BPCAs were separated and quantified using an HPLC system (UltiMate 3000, Thermo Fisher, Germany) (CV  More

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A diverse and active DNA virosphereWe first leveraged two existing metagenomes that were constructed from the Konza native prairie soil14,15 to screen for viral sequences at the site. Each of the metagenomes was obtained from a composite of all the replicate soils collected at ambient field moisture conditions. One of the metagenomes was de novo assembled from deep sequence data (1.1 Tb)14 and the second was a hybrid assembly of short and long reads (267.0 Gb)16. The combination of the two metagenomes was used to maximize the coverage of viral sequences from the Konza prairie site. To balance between the detection limits of the viral detection tools and the wide range of viral genome size, the viral contigs > 2.5 kb in length were combined with those obtained from screening of the two largest public viral databases (i.e., IMG/VR17 and NCBI Virus16) to further increase the coverage of DNA viral sequences. We acknowledge that the length cutoff of 2.5 kb would preclude detection of some ssDNA viruses with small segmented genome sizes (e.g., Nanoviridae18). As a result, a DNA viral database for the site was curated that included 726,108 de-replicated viral contigs. The DNA viral database then served as a scaffold for mapping of metatranscriptome and metaproteome datasets to determine the activities of soil DNA viruses and their responses to differences in soil moisture. This approach was also recently applied to detect the transcriptional activity of marine prokaryotic and eukaryotic viruses19,20,21,22 and giant viruses in soil5.The metatranscriptome reads from both wet and dry treatments were mapped to a total of 416 unique DNA viral contigs using stringent criteria (% sequence identity > 95% and % sequence coverage > 80%). The 416 DNA viral contigs with an average sequence length of 19 kb were highly diverse and grouped into 139 clusters, with 111 of the clusters being singletons (Supplementary Data 1).We aimed to assign putative host taxa to the viral clusters by combining several approaches: CRISPR spacer matching, and screening for host and viral sequence similarities to respective databases (details in ‘Methods’). As a result, we assigned putative viral host taxa to 160 out of the 416 transcribed DNA viral contigs. Some of these were assigned to more than one host (Supplementary Data 1), resulting in a total of 181 virus–host pairings (Fig. 1a). Of these, 79 host–virus pairs were detected only in the dry soil treatment, 51 were only in the wet soil treatment, and an additional 51 were found in both dry and wet treatments (Fig. 1a). Consistent with previous reports4, the majority of the transcribed DNA viral contigs were annotated as bacteriophage sequences. Different sets of transcribed DNA viral contigs were unique to wet or dry soils and assigned to specific hosts at the phylum level, whereas others were shared (Fig. 1a). However, the dominant soil taxa, i.e., Proteobacteria and Actinobacteria that were previously identified by 16S rRNA gene sequencing in this soil environment, were predicted as hosts under both wet and dry conditions (Supplementary Fig. 1a). Eukaryotic DNA viruses, such as Bracovirus and Ichnovirus belonging to a family of insect viruses within the Polydnaviridae family, were also transcribed in the soils (Fig. 1a and Supplementary Data 1). Most of these insect viruses were only detected in dry soil conditions. These differences in virus–host pairings suggest that some of the respective hosts were impacted differently by the dry and wet incubation conditions.Fig. 1: Transcribed DNA viral communities and their responses to wet and dry soil conditions.a An alluvium plot that illustrates pairings of the transcribed DNA viral contigs to putative host phyla. The transcribed DNA viral community was comprised of viral contigs from the curated DNA viral databases that were mapped by quality-filtered metatranscriptomic reads. The alluvia are colored by host taxa (first x axis of each sub-panel) assigned to respective transcribed DNA viral contigs (second x axis of each sub-panel). b A Venn diagram showing the number of unique transcribed DNA viral contigs detected in both wet and dry soils and ones exclusively detected in one of the soils. c Number of unique DNA viral contigs detected. A t-Test shows significantly more DNA contigs were transcribed in dry soil (p = 0.044). d Number of transcripts that mapped to the DNA viral contigs. For panels (c) and (d), the two independent field sites of Konza Experimental Field Station are indicated as site A (circles) and site C (triangles), with the wet soil in blue and dry soil in red.Full size imageThere were 21 DNA viral contigs that were assigned to hosts across multiple bacterial phyla suggesting the presence of viral generalists1,23 (Supplementary Data 1). We recognize that host assignment based on CRISPR spacer matching, however, is limited to detection of recent or historical virus–host interactions that were captured at the time of sampling24. As bioinformatics assignment of virus–host linkages only suggests possible pairings based on sequence features, there are also chances of introducing false positives. However, we applied the most stringent criteria possible to provide confident host assignments.Increased activity of a subset of DNA viruses in wet soilSoil moisture has a strong influence on the community structures of transcribed DNA viruses. The majority of the transcriptionally active DNA viral contigs were unique to wet or dry conditions, with only 111 viral contigs (~ 26.7%) detected in both wet and dry soils, suggesting that the different soil moisture conditions may shape the activity of the DNA viral community differently (Fig. 1b). Interestingly, although a significantly higher number of transcribed DNA viral contigs were detected in dry soils (Fig. 1b, c), the levels of transcriptional activity were significantly higher (based on the normalized abundance of RNA reads that mapped to the viral contigs) for DNA viruses in wet soils irrespective of sampling site location (Fig. 1d). DNA viral contigs with mapped transcripts could represent either prophages that are passively replicated along with their host genomes, or (lytic) viruses that are actively regulating early/middle/late expression of viral gene clusters25. In soil, a lysogenic lifestyle is considered to be an adaptive strategy for viruses to cope with long periods of low host activity26,27. Therefore, the 1.5-fold increase in the number of transcribed DNA viral contigs representing transcriptionally active DNA viruses, but with lower levels of overall transcription, in dry soil suggests that the increase was due to a higher prevalence of lysogeny in dry conditions. This hypothesis is strengthened by our finding of a 20-fold increase in transcripts for lysogenic markers (i.e., integrase and excisionase) in one of our replicates (A-2) in dry compared to wet conditions (Supplementary Data 2). High number of lysogenic phages were also previously reported in dry Antarctic soils using a cultivation-independent induction assay28. By contrast, under wet soil conditions we found a 2-fold increase in transcription of fewer viral contigs representing a subset of DNA viruses, suggesting that those viruses were more transcriptionally active in response to higher soil moisture. In addition, there was a higher correlation between prokaryotic abundances, as estimated by 16S rRNA gene sequencing, with DNA viral transcript counts in wet soils (R2 = 0.593, Supplementary Fig. 1d) in comparison to dry soils (R2 = 0.069, Supplementary Fig. 1d), supporting this hypothesis.We then identified which soil DNA viruses were most transcriptionally active and how they responded to the differences in soil moisture. As the majority of the transcribed DNA viral contigs (97%) were environmental viruses with unclassified taxonomy assignment, we were not able to calculate the taxonomic abundance of each and instead compared the differential abundances of the transcribed viral contigs. There were four DNA viral contigs with significantly different levels of transcription under wet and dry conditions (VC_1, VC_19, VC_282, VC_412; Fig. 2a). Contigs VC_1 and VC_19 correspond to unclassified viral contigs deposited in IMG/VR (identifiers of ‘REF:2547132004_2547132004’ and ‘3300010038_Ga0126315_10000854’) that were previously detected in metagenomes from the Rifle site29 and from serpentine soil in the UC McLaughlin Reserve30, respectively. Contigs VC_282 and VC_412 were extracted from our Kansas metagenomes. Contigs VC_1 and VC_19 had significantly higher levels of transcriptional activity in wet soils compared to dry soils (p  More