Diversity in the soil virosphere: to infinity and beyond?

Roux, Simon; Emerson, Joanne B.

doi:10.1016/j.tim.2022.05.003

Cited by 47 publications

(49 citation statements)

References 107 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, the fact that we could still discern clear differences in viral community composition between healthy and diseased plants suggests that we could capture the representative variation of more common viral taxa. Resuspending and enriching phages in soil samples before isolation and sequencing of phage metagenome libraries can be used to increase the viral taxonomic resolution to assess the role of rarer viral taxa and to assemble larger viral contigs for the identification of viral auxiliary metabolism genes [ 16 , 25 , 55 ]. This will also enable clearer identification of prophages and lysogenic phages from bacterial metagenomes to assess their role in bacteria-phage interactions in rhizosphere microbiomes.…”

Section: Discussionmentioning

confidence: 99%

Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease

et al. 2023

View full text Add to dashboard Cite

Background Bacterial viruses, phages, play a key role in nutrient turnover and lysis of bacteria in terrestrial ecosystems. While phages are abundant in soils, their effects on plant pathogens and rhizosphere bacterial communities are poorly understood. Here, we used metagenomics and direct experiments to causally test if differences in rhizosphere phage communities could explain variation in soil suppressiveness and bacterial wilt plant disease outcomes by plant-pathogenic Ralstonia solanacearum bacterium. Specifically, we tested two hypotheses: (1) that healthy plants are associated with stronger top-down pathogen control by R. solanacearum-specific phages (i.e. ‘primary phages’) and (2) that ‘secondary phages’ that target pathogen-inhibiting bacteria play a stronger role in diseased plant rhizosphere microbiomes by indirectly ‘helping’ the pathogen. Results Using a repeated sampling of tomato rhizosphere soil in the field, we show that healthy plants are associated with distinct phage communities that contain relatively higher abundances of R. solanacearum-specific phages that exert strong top-down pathogen density control. Moreover, ‘secondary phages’ that targeted pathogen-inhibiting bacteria were more abundant in the diseased plant microbiomes. The roles of R. solanacearum-specific and ‘secondary phages’ were directly validated in separate greenhouse experiments where we causally show that phages can reduce soil suppressiveness, both directly and indirectly, via top-down control of pathogen densities and by alleviating interference competition between pathogen-inhibiting bacteria and the pathogen. Conclusions Together, our findings demonstrate that soil suppressiveness, which is most often attributed to bacteria, could be driven by rhizosphere phage communities that regulate R. solanacearum densities and strength of interference competition with pathogen-suppressing bacteria. Rhizosphere phage communities are hence likely to be important in determining bacterial wilt disease outcomes and soil suppressiveness in agricultural fields.

show abstract

Section: Discussionmentioning

confidence: 99%

Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease

et al. 2023

View full text Add to dashboard Cite

show abstract

“…Finally, beyond the apparent dominance of ssRNA Leviviricetes bacteriophages in ERW soils, our phylogenetic analysis suggests that a significant number of RNA viruses detected in this work infect fungal, plant and animal hosts. Among these, most of them display some similarity to other uncultivated soil viruses, with no match with isolated references, consistent with the existence of a "global soil virosphere" still only partially sampled 21,29 . Interestingly, most of these viruses were predicted to infect fungal hosts, suggesting that the diversity of these mycoviruses may also be largely under-characterized 65 .…”

Section: Discussionmentioning

confidence: 93%

“…Viruses infecting bacteria and archaea (hereafter referred to as phages) are the most common and diverse group of viruses identified in soil [19][20][21][22] , and can harbor various virion morphologies and genome types including double-stranded DNA (dsDNA), single-stranded DNA (ssDNA), single-stranded RNA (ssRNA), and double-stranded RNA (dsRNA) genomes 25 . Soil viruses are highly abundant and diverse, however current public databases still capture only a fraction of this diversity (mainly dsDNA viruses) 7,[27][28][29] , due to a combination of biological biases and methodological limitations.…”

Section: Introductionmentioning

confidence: 99%

“…Soil viruses are highly abundant and diverse, however current public databases still capture only a fraction of this diversity (mainly dsDNA viruses) 7,[27][28][29] , due to a combination of biological biases and methodological limitations. Virus genome representation in public database is also biased towards dsDNA phages, which represent the overwhelming majority of viruses reported in soil to date 21,22 , while our current knowledge of the diversity and ecological role of soil RNA and ssDNA viruses remains limited 12,13,[30][31][32] .…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Self Cite

View full text Add to dashboard Cite

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.

show abstract

“…With up to 10 10 viral particles per gram of soil, viruses are assumed to be influential in terrestrial ecosystems too [5][6][7][8][9][10] , but viral impacts on soil ecology and biogeochemistry are just beginning to be explored. Although methodological barriers for soil viral community analyses have largely been overcome [10][11][12][13] , the recent advent of large-scale viral sizefraction metagenomics (viromics) in soil has heralded new challenges associated with extreme soil viral diversity 12,[14][15][16][17][18] .…”

Section: Introductionmentioning

confidence: 99%

Viral but not bacterial community succession is characterized by extreme turnover shortly after rewetting dry soils

Santos‐Medellín

Blazewicz

Pett‐Ridge

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

As central members of soil trophic networks, viruses have the potential to drive substantial microbial mortality and nutrient turnover. Pinpointing viral contributions to terrestrial ecosystem processes remains a challenge, as temporal dynamics are difficult to unravel in the spatially and physicochemically heterogeneous soil environment. In Mediterranean grasslands, the first rainfall after seasonal drought provides an ecosystem reset, triggering microbial activity during a tractable window for capturing short-term dynamics. Here, we simulated precipitation in microcosms from four distinct, dry grassland soils and generated 144 viromes and 84 metagenomes to characterize viral, prokaryotic, and relic DNA dynamics over 10 days. Vastly different viral communities in each soil followed remarkably similar successional trajectories. Wet-up triggered a significant increase in viral abundance and richness, followed by extensive compositional turnover. While temporal turnover in prokaryotic communities was much less pronounced, differences in the relative abundances of Actinobacteria (enriched in dry soils) and Proteobacteria (enriched in wetted soils) matched those of their predicted phages, indicating viral predation of dominant bacterial taxa. Rewetting also rapidly depleted relic DNA, which subsequently re-accumulated, indicating substantial new microbial mortality in the days after wet-up, particularly of the taxa putatively under phage predation. Production of abundant, diverse viral particles via microbial host cell lysis appears to be a conserved feature of the early response to soil rewetting, and results suggest the potential for "Cull-the-Winner" dynamics, whereby viruses infect and cull but do not decimate dominant host populations.

show abstract

Diversity in the soil virosphere: to infinity and beyond?

Cited by 47 publications

References 107 publications

Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease

Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease

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

Viral but not bacterial community succession is characterized by extreme turnover shortly after rewetting dry soils

Contact Info

Product

Resources

About