Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Muscatt, George; Hilton, Sally; Raguideau, Sébastien; Teakle, Graham R.; Lidbury, Ian; Wellington, Elizabeth M. H.; Quince, Christopher; Millard, Andrew; Bending, Gary D.; Jameson, Eleanor

doi:10.1101/2022.04.22.488307

Cited by 3 publications

(11 citation statements)

References 114 publications

(135 reference statements)

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“…Indeed, fine roots and hyphae have been reported to a depth of at least 2 m at the same study site [46]. The consequence of growing crop roots on the structures of both DNA and RNA soil viral communities has been demonstrated previously [13].…”

Section: Discussionmentioning

confidence: 70%

“…Viruses can carry and express AMGs during infection to modulate the host’s metabolism and fitness, and promote their co-existence [2–6]. Moreover, viral-encoded AMGs have the potential to affect soil biogeochemistry, with viruses previously implicated in soil carbon processing [13, 18, 19, 34, 99, 125]. In this study, we detected viruses throughout the soil depth profile carrying CAZymes associated with both carbohydrate anabolism and catabolism (Table S5).…”

Section: Discussionmentioning

confidence: 99%

“…Integral to understanding soil viral ecology are the fundamentals of viral dispersal, prevalence, and persistence. The consequence of these factors is demonstrated by the structuring of viral communities across gradients of space [14–18], time [13, 16, 17], and root/soil compartment [13, 19]. However, most ecological studies have focussed on surface soils, rendering subsurface viral communities markedly underexplored.…”

Section: Introductionmentioning

confidence: 99%

“…Lysogenic infections can have significant impacts on the ecology and evolution of their host communities (hereafter referred to as “eco-evolutionary interactions”) [30]. While temperate viruses, capable of lysogeny, have been predicted to dominate in soils [31–33], relevant metagenomic studies have failed to corroborate this [12, 13, 34]. The argument for such increased lysogeny, namely the reduced access to viable hosts [28, 29, 35], has a stronger case in subsurface soil.…”

Section: Introductionmentioning

confidence: 99%

“…Despite an appreciation for the ecological roles of viruses in marine ecosystems, the relevant functions of viruses in terrestrial ecosystems have received less attention. To resolve this, recent methodological developments have provided the means to investigate soil viral ecology through metagenomics [10][11][12], and we are beginning to uncover the ecosystem-level impacts of soil viruses [13].…”

Section: Introductionmentioning

confidence: 99%

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Ecological and evolutionary patterns of virus-host interactions throughout a grassland soil depth profile

Muscatt

Cook

Millard

et al. 2022

Preprint

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Background:Soil microbes play pivotal roles in global carbon cycling, however the fundamental interactions between microbes and their infecting viruses remain unclear. This is exacerbated with soil depth, where the patterns of viral dispersal, ecology, and evolution are markedly underexplored. To investigate viral communities across soil depth, we leveraged a publicly available metagenomic data set sampled from grassland soil in northern California.Results:10,196 non-redundant vOTUs were recovered from soil sampled from 20 cm to 120 cm below the surface. Viral prevalence was high throughout the soil depth profile, with viruses infecting dominant soil phyla, includingActinomycetota. Contrary to leading hypotheses, lysogeny did not dominate in the soil viral communities. Viral diversity was investigated at both the population-level (i.e., macro diversity) and strain-level (i.e., micro diversity) to reveal diverse ecological and evolutionary patterns of virus-host interactions in surface and subsurface soil.Conclusions:By investigating viral micro diversity in soil for the first time, we have uncovered patterns of antagonistic co-evolution across both surface and subsurface soils. Furthermore, we have provided evidence of soil viruses augmenting the remineralisation of soil carbon. While we continue to yield a more comprehensive understanding of soil viral ecology, our work appeals to future researchers to continue to investigate subsurface viral communities.

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Section: Discussionmentioning

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ecological and evolutionary patterns of virus-host interactions throughout a grassland soil depth profile

Muscatt

Cook

Millard

et al. 2022

Preprint

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Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

Coclet

Sørensen

Karaöz

et al. 2023

Preprint

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Viruses, including phages, impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time, and their response to strong seasonal change in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental DNA and RNA viruses, including phages, across dynamics seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes. We identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of RNA viruses target fungal hosts and a large and unsuspected diversity of positive single-stranded RNA phages (Leviviricetes), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active phages which changed across seasons, consistent with a 'seed-bank' viral community structure in which new phage activity, for example replication and host lysis, is sequentially triggered by changes in environmental conditions. Zooming in at the population level, we further identified virus-host dynamics matching two existing ecological models: 'Kill-The-Winner' which proposes that lytic phages are actively infecting abundant bacteria, and 'Piggyback-The-Persistent' which argues that when the host is growing slowly it is more beneficial to remain in a lysogenic state. The former was associated with summer months of high and rapid microbial activity, and the latter to winter months of limited and slow host growth. Taken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. Moving forward, while as our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry.

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Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

Coclet,

Sorensen,

Karaoz

et al. 2023

Microbiome

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Background Viruses impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time and their response to strong seasonal changes in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental soil DNA and RNA viruses, focusing especially on bacteriophages, across dynamics’ seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes. Results We identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of fungal RNA viruses, and a large and unsuspected diversity of positive single-stranded RNA phages (Leviviricetes), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active DNA and RNA phages that changed across seasons, consistent with a “seed-bank” viral community structure in which new phage activity, for example, replication and host lysis, is sequentially triggered by changes in environmental conditions. At the population level, we further identified virus-host dynamics matching two existing ecological models: “Kill-The-Winner” which proposes that lytic phages are actively infecting abundant bacteria, and “Piggyback-The-Persistent” which argues that when the host is growing slowly, it is more beneficial to remain in a dormant state. The former was associated with summer months of high and rapid microbial activity, and the latter with winter months of limited and slow host growth. Conclusion Taken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. As our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry.

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Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Cited by 3 publications

References 114 publications

Ecological and evolutionary patterns of virus-host interactions throughout a grassland soil depth profile

Ecological and evolutionary patterns of virus-host interactions throughout a grassland soil depth profile

Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

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