An empirical model of carbon flow through marine viruses and microzooplankton grazers

Talmy, David; Beckett, Stephen J.; Taniguchi, Darcy A. A.; Brussaard, Corina P. D.; Weitz, Joshua S.; Follows, Michael J.

doi:10.1111/1462-2920.14626

Cited by 24 publications

(31 citation statements)

References 51 publications

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“…The accuracy of the model could be improved by adding the molecular mechanisms leading to the formation of new lysogens, which has been modeled at single strain-level but proven hard to incorporate into ecological scenarios (Steward and Levin 1984; Wang and Goldenfeld 2010; Maslov and Sneppen 2017; Wahl et al 2018; Weitz et al 2019; Chaudhry et al 2019). The accuracy could be also improved by incorporating by incorporating specific predator and immune system pressure (Thingstad and Lignell 1997; Thingstad 2000; Winter et al 2010; Dwayne et al 2017; Caron et al 2017; Talmy et al 2019), variable energy sources (Thingstad and Lignell 1997; Weitz et al 2015), and ecosystem-specific ranges for phage-bacteria traits and nested viral-microbial networks (Flores et al 2011; Thingstad et al 2014; Gao et al 2017; Hendricks 1972; Kirchman 2016; De Paepe and Taddei 2006).…”

Section: Discussionmentioning

confidence: 99%

Phage and bacteria diversification through a prophage acquisition ratchet

Anthenelli

Jasien

Edwards

et al. 2020

Preprint

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16Lysogeny is prevalent in the microbial-dense mammalian gut. This contrasts the classi-17 cal view of lysogeny as a refuge used by phages under poor host growth conditions. Here 18 we hypothesize that as carrying capacity increases, lysogens escape phage top-down control 19 through superinfection exclusion, overcoming the canonical trade-off between competition and 20 resistance. This hypothesis was tested by developing an ecological model that combined lytic 21 and lysogenic communities and a diversification model that estimated the accumulation of 22 prophages in bacterial genomes. The ecological model sampled phage-bacteria traits stochas-23 tically for communities ranging from 1 to 1000 phage-bacteria pairs, and it included a fraction 24 of escaping lysogens proportional to the increase in carrying capacity. The diversification 25 model introduced new prophages at each diversification step and estimated the distribution 26 of prophages per bacteria using combinatorics. The ecological model recovered the range of 27 abundances and sublinear relationship between phage and bacteria observed across eleven 28 ecosystems. The diversification model predicted an increase in the number of prophages per 29 genome as bacterial abundances increased, in agreement with the distribution of prophages 30 on 833 genomes from marine and human-associated bacteria. The study of lysogeny pre-31 sented here offers a framework to interpret viral and microbial abundances and reconciles the 32 Kill-the-Winner and Piggyback-the-Winner paradigms in viral ecology.33The human gut contains one of the highest concentrations of bacteria and phages-viruses that 35 infect bacteria-across ecosystems (Knowles et al. 2016; Wigington et al. 2016; Parikka et al. 2017). 36 This high concentration of microbes is sustained by the daily supply of nutrient-rich compounds 37 received from food intake and microbial metabolism (Blaut 2011; Cotillard et al. 2013; Mirzaei 38 and Maurice 2017). In other ecosystems-mostly aquatic environments-an increase of resources 39 has been linked to bacterial growth and phage lytic life cycle. This phage strategy produces new 40 phage particles upon infection and subsequently bursts the bacterial host (lysis). Combined with 41 the bacterial growth, the lytic life cycle ensures a rapid turnover of nutrients charateristic of the 42 kill-the-winner (KtW) dynamics (Maurice et al. 2011; Brum et al. 2016; Thingstad and Lignell 43 1997). In the nutrient-rich and microbial dense gut ecosystem, thus, one would expect a similar 44 phage lytic strategy. 45 Yet the lysogenic life cycle seems to be prevalent in the gut, where upon infection the phage 46 genome integrates in the bacterial host as a prophage, forming a phage-bacteria symbiont called 47 lysogen. Markers of lysogeny have been observed in viral genomic and metagenomic data from 48 healthy adults (Furuse et al. 1983; Letarov and Kulikov 2009; Reyes et al. 2010; Minot et al.

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Section: Discussionmentioning

confidence: 99%

Phage and bacteria diversification through a prophage acquisition ratchet

Anthenelli

Jasien

Edwards

et al. 2020

Preprint

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“…When building from the standard Lotka-Volterra core equations, including a consumer and a virus that both target the same resource generally leads to a collapse, with one outcompeting the other (Weitz, 2016). To maintain coexistence, models have invoked complex, multi-taxa food web dynamics, such as in the "kill the winner" model (Thingstad, 2000), higher order mortality terms for stability (Talmy et al, 2019), or ecological trade-offs (Record et al, 2016). Direct consumption of viruses by protists adds a new interaction that actually stabilizes the three-equation virus-host-consumer model without requiring a more complex model (Hsu et al, 2015).…”

Section: Implications For the Functioning Of The Marine Microbial Loopmentioning

confidence: 99%

Single Cell Genomics Reveals Viruses Consumed by Marine Protists

et al. 2020

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The predominant model of the role of viruses in the marine trophic web is that of the "viral shunt," where viral infection funnels a substantial fraction of the microbial primary and secondary production back to the pool of dissolved organic matter. Here, we analyzed the composition of non-eukaryotic DNA associated with individual cells of small, planktonic protists in the Gulf of Maine (GoM) and the Mediterranean Sea. We found viral DNA associated with a substantial fraction cells from the GoM (51%) and the Mediterranean Sea (35%). While Mediterranean SAGs contained a larger proportion of cells containing bacterial sequences (49%), a smaller fraction of cells contained bacterial sequences in the GoM (19%). In GoM cells, nearly identical bacteriophage and ssDNA virus sequences where found across diverse lineages of protists, suggesting many of these viruses are non-infective. The fraction of cells containing viral DNA varied among protistan lineages and reached 100% in Picozoa and Choanozoa. These two groups also contained significantly higher numbers of viral sequences than other identified taxa. We consider mechanisms that may explain the presence of viral DNA in protistan cells and conclude that protistan predation on free viral particles contributed to the observed patterns. These findings confirm prior experiments with protistan isolates and indicate that the viral shunt is complemented by a viral link in the marine microbial food web. This link may constitute a sink of viral particles in the ocean and has implications for the flow of carbon through the microbial food web.

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“…Modeling marine food webs on global scales remains a challenge because ecological processes are temporally and spatially variable. Data quantifying food web processes are scarce and model parameterizations are simplified representations of the functioning of biological populations and communities (Nicholson et al, 2018;Talmy et al, 2019). Although there are studies that aim to predict either the bulk sinking POC flux or the various pathways for POC flux from satellite data (Siegel et al, 2014;Archibald et al, 2019), less work addresses how different passive sinking pathways function together.…”

Section: Introductionmentioning

confidence: 99%