Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing

Daly, Rebecca A.; Roux, Simon; Borton, Mikayla A.; Morgan, David M. L.; Johnston, Michael D.; Booker, Anne E.; Hoyt, David; Meulia, Tea; Wolfe, Richard A.; Hanson, Andrea; Mouser, Paula J.; Moore, Joseph; Wunch, Kenneth; Sullivan, Matthew B.; Wrighton, Kelly; Wilkins, Michael J.

doi:10.1038/s41564-018-0312-6

Cited by 94 publications

(118 citation statements)

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“…The unique CRISPR arrays indicate that closely related species may be infected by different viruses with species specificity [71]. However, some viral populations have been reported to have broad host ranges [72]. Divergent evolution or strain level microdiversity may also explain distinct CRISPR-Cas systems [73].…”

Section: Discussionmentioning

confidence: 99%

Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

Bhatnagar

Cowley

Kopf³

et al. 2019

Preprint

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31Phototrophic microbial mats commonly contain multiple phototrophic lineages that coexist based 32 on their light, oxygen and nutrient preferences. Here we show that similar coexistence patterns 33 and ecological niches can occur in suspended phototrophic blooms of an organic-rich estuary. 34 The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper 35 part of the bloom was dominated by aerobic phototrophic Cyanobacteria, the middle and lower 36 parts were dominated by anoxygenic purple sulfur bacteria (Chromatiales) and green sulfur 37 bacteria (Chlorobiales), respectively. We found multiple uncultured phototrophic lineages and 38 present metagenome-assembled genomes of two uncultured organisms within the Chlorobiales. 39 Apparently, those Chlorobiales populations were affected by Microviridae viruses. We suggest a 40 sulfur cycle within the bloom in which elemental sulfur produced by phototrophs is reduced to 41 sulfide by Desulfuromonas sp. These findings improve our understanding of the ecology and 42 ecophysiology of phototrophic blooms and their impact on biogeochemical cycles. 43Background 44 Estuarine and coastal water bodies are dynamic and ubiquitous ecosystems that are often 45 characterized by the mixing of terrestrial freshwater and ocean saltwater. Brackish habitats can 46 have striking physical and chemical characteristics that differ from both fresh and saltwater 47 ecosystems [1,2]. Brackish ecosystems are very diverse and support large microbial and 48 macrobial communities [1]. Estuaries also provide crucial ecosystem services, the most salient of 49 which are trapping and filtering terrestrial runoffs and pollutants before they enter the oceans, 50 coastal protection, erosion control and habitat-fishery linkages [3][4][5][6]. 51Estuaries harbor abundant and diverse microbial communities that form the basis of a complex 52 food chain by fixing carbon dioxide through photosynthesis or chemosynthesis [7][8][9]. 53Additionally, carbon introduced to estuaries as organic matter from the oceans or land can be 54 remineralized by heterotrophic microbial communities [10][11][12]. The decomposition of sulfur 55 containing organic compounds through fermentation can lead to the production of sulfide in 56 estuarine sediments [13]. Furthermore, sulfate brought into estuaries by ocean waters can be used 57 by sulfate reducers, which reduce sulfate into elemental sulfur or sulfide [13,14]. Sulfate 58 introduced by ocean water and sulfide released from the sediments form gradients in the water 59 column that cause a chemocline in the brackish water column [15]. Additionally, estuaries and 60 coastal marshes often exhibit a halocline, i.e. a change in salinity, and the depletion of oxygen in 61 the water column can create an oxycline [16,17]. Overlapping gradients, e.g. in salinity, light 62 availability, as well as oxygen and sulfide concentration can create habitats and niches that favor 63 certain microbial communities and conversely microbial communiti...

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Section: Discussionmentioning

confidence: 99%

Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

Bhatnagar

Cowley

Kopf³

et al. 2019

Preprint

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“…Phage infection is dependent on encountering a suitable bacterial cell after which the phage genome is injected into the host cell entering an intracellular stage. As obligate predators of prokaryotes, lytic phages may reproduce through a lytic life cycle resulting in the destruction of the host cell following production of progeny phage (Williamson et al ., ; Daly et al ., ). Alternatively, temperate phages may reproduce lytically or via a lysogenic life cycle in which the phage genome is stably integrated into the host genome and replicated as the host cell grows and divides.…”

Section: Introductionmentioning

confidence: 97%

“…Viral population dynamics and their ecological correlations with biotic and environmental processes in terrestrial subsurface are under‐investigated relative to freshwater, marine and aquatic sedimentary environments. However, several notable studies suggest that viruses are abundant, diverse and active members of aquatic and terrestrial ecosystems (Williamson et al ., ; ; Narr et al ., ; Pratama and van Elsas, ; Daly et al ., ). The purpose of this study was to determine the response of bacterial communities and their associated viral assemblages to stimulated anaerobic Fe(III)‐bioreduction during electron donor addition in laboratory‐scale bioremediation column experiments.…”

Section: Introductionmentioning

confidence: 97%

Viral and bacterial community responses to stimulated Fe(III)‐bioreduction during simulated subsurface bioremediation

Liang

Zhuang

Löffler

et al. 2019

Environmental Microbiology

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Summary The delivery of fermentable substrate(s) to subsurface environments stimulates Fe(III)‐bioreduction and achieves detoxification of organic/inorganic contaminants. Although, much research has been conducted on the microbiology of such engineered systems at lab and field scales, little attention has been given to the phage‐host interactions and virus community dynamics in these environments. The objective was to determine the responses of soil bacterial communities and viral assemblages to stimulated anaerobic Fe(III)‐bioreduction following electron donor (e.g. acetate) addition. Microbial communities, including viral assemblages, were investigated after 60 days of Fe(III)‐bioreduction in laboratory‐scale columns continuously fed with acetate‐amended artificial groundwater. Viral abundances were greatest in the influent section and decreased along the flow path. Acetate availability was important in influencing bacterial diversity, microbial interactions and viral abundance and community composition. The impact of acetate addition was most evident in the influent section of the columns. The increased relative abundance of Fe(III)‐reducing bacteria coincided with an increase in viral abundance in areas of the columns exhibiting the most Fe(III) reduction. The genetic composition of viruses in these column sections also differed from the control column and distal sections of acetate‐treated columns suggesting viral communities responded to biostimulated Fe(III)‐bioreduction.

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“…The diversity of CRISPR alleles in natural, experimental and simulated populations has been explored [30][31][32][33][34]. It has been shown, for example, that increased strain diversity of Pseudomonas aeruginosa (with strains being clones with different spacer compositions) promotes the ability of the bacterium to control the DMS3vir virus [32].…”

Section: Introductionmentioning

confidence: 99%

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification

Pilosof

Alcalá-Corona

Wang

et al. 2019

Preprint

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As a heritable sequence-specific adaptive immune system, CRISPR-Cas is a powerful force shaping strain diversity in host-virus systems. While the diversity of CRISPR alleles has been explored, the associated structure and dynamics of host-virus interactions has not. We develop theory on the role of CRISPR immunity in mediating the interplay between host-virus interaction structure and eco-evolutionary dynamics in a computational model and three natural systems. We show that the structures of networks describing who infects whom and who is protected from whom are modular and weighted-nested, respectively. The dynamic interplay between these networks influences transitions between dynamical regimes of virus diversification and host control,leading to eventual virus extinction. The three empirical systems exhibit weighted nestedness, a pattern our theory shows is indicative of viral control by hosts. Previously missing from studies of microbial host-pathogen systems, the protection network plays a key role in the coevolutionary dynamics. IntroductionThe structure of complex ecological communities is clearly non-random. It is generally argued that interaction structure affects the stability of communities to perturbations [1-3] and arises from coevolutionary dynamics between interacting partners [4][5][6][7], yet the structure-dynamics nexus remains a long-standing central question in community and network ecology. Host-parasite infection networks, in which interaction structure represents 'who infects whom', have been typically described as modular, nested, or both [8,9]. Modularity concerns patterns of specificity, in which the network is partitioned into modules of hosts and parasites that interact densely with each other but sparsely with those outside the group. Nestedness concerns instead patterns of specialization, and describes a network structure in which specialist hosts are infected by subsets of parasites that in turn also infect the more generalist hosts [8,9].Common to all host-parasite network studies is a dominant focus on patterns of infection. Infection structure should critically depend however on the genetic basis of resistance of hosts to pathogens [10]. The emergence of network structure from immune selection has been shown in pathogens of humans such as Plasmodium falciparum [11, 12]. In particular, strain theory developed for pathogens with multilocus encoding of antigens posits that negative frequency dependent selection, mediated by competition for hosts through cross-immunity, can structure pathogen populations into clusters of strains with limited overlap of antigenic repertoires [11][12][13][14][15]. Parasites with 2 . CC-BY-NC-ND 4.0 International license is made available under a resistance by surface mutation can arise quickly to take over CRISPR or restriction-modification systems in providing immunity. This experimental and theoretical evidence for advantages of surface modification may entail strong fitness costs under natural conditions because mutations in surface receptors such a...

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Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing

Cited by 94 publications

References 64 publications

Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

Viral and bacterial community responses to stimulated Fe(III)‐bioreduction during simulated subsurface bioremediation

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification

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