Viral infection of algal blooms leaves a unique metabolic footprint on the dissolved organic matter in the ocean

Kuhlisch, Constanze; Schleyer, Guy; Shahaf, Nir; Vincent, Flora; Schatz, Daniella; Vardi, Assaf

doi:10.1126/sciadv.abf4680

Cited by 52 publications

(44 citation statements)

References 64 publications

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“…This suggests that the possible lytic event was not the result of lysogenic induction (or at least that any lysogenic induction was incomplete). Such variable virus expression has recently been observed in other experimental systems, including an Emiliania huxleyi bloom induced in mesocosms, where researchers noted highly variable virus expression between replicate samples ( Kuhlisch et al, 2021 ). In a likewise manner, their observations were tied to variability in host metrics, including chlorophyll a and metabolites.…”

Section: Discussionmentioning

confidence: 68%

“…In the current experiments, however, at least some of this variability can potentially be attributed to subtle shifts in the microbiome of the target community, which can occur in either natural systems or in non-axenic lab cultures ( Pound et al, 2021a ). Moreover, as recently shown in other systems ( Kuhlisch et al, 2021 ; Vincent et al, 2021 ) we can take advantage of the variability between replicates to learn more about our system.…”

Section: Discussionmentioning

confidence: 90%

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Changes in Microbiome Activity and Sporadic Viral Infection Help Explain Observed Variability in Microcosm Studies

et al. 2022

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The environmental conditions experienced by microbial communities are rarely fully simulated in the laboratory. Researchers use experimental containers (“bottles”), where natural samples can be manipulated and evaluated. However, container-based methods are subject to “bottle effects”: changes that occur when enclosing the plankton community that are often times unexplained by standard measures like pigment and nutrient concentrations. We noted variability in a short-term, nutrient amendment experiment during a 2019 Lake Erie, Microcystis spp. bloom. We observed changes in heterotrophic bacteria activity (transcription) on a time-frame consistent with a response to experimental changes in nutrient availability, demonstrating how the often overlooked microbiome of cyanobacterial blooms can be altered. Samples processed at the time of collection (T0) contained abundant transcripts from Bacteroidetes, which reduced in abundance during incubation in all bottles, including controls. Significant biological variability in the expression of Microcystis-infecting phage was observed between replicates, with phosphate-amended treatments showing a 10-fold variation. The expression patterns of Microcystis-infecting phage were significantly correlated with ∼35% of Microcystis-specific functional genes and ∼45% of the cellular-metabolites measured across the entire microbial community, suggesting phage activity not only influenced Microcystis dynamics, but the biochemistry of the microbiome. Our observations demonstrate how natural heterogeneity among replicates can be harnessed to provide further insight on virus and host ecology.

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Section: Discussionmentioning

confidence: 68%

Section: Discussionmentioning

confidence: 90%

Changes in Microbiome Activity and Sporadic Viral Infection Help Explain Observed Variability in Microcosm Studies

et al. 2022

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“…There exists a large amount of uncertainty regarding the loss rates caused by these processes. It is difficult to constrain the maximum rates of lysis and exudation, as it is typically not straightforward to distinguish between the DOM released through these processes (but see Ma et al, 2018; Kuhlisch et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Growth, organic matter release, aggregation and recycling during a diatom bloom: A model-based analysis of a mesocosm experiment

Kerimoglu

Hintz

Lücken

et al. 2022

Preprint

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Mechanisms terminating phytoplankton blooms are often not well understood. Potentially involved processes such as consumption by grazers, flocculation, and viral lysis each have different post-bloom consequences on the processing of the organic material, therefore it is important to develop a better understanding of the relevance of these processes, and potential interactions between them. In this study, we present a model-based analysis of a spring bloom observed in a mesocosm experiment. The intermediate-complexity (27-state variable) numerical model we extended from an earlier version to this end can resolve C, N, P and Si cycles, and relevant processes like formation of various organic material size classes (low and high molecular weight (hereafter small and large) dissolved organic carbon (DOC), transparent exopolymer particles (TEP), and small/large detritus) and their degradation by two bacterial sub-communities (free-living and particle-attached) and planktonic protists (heterotrophic flagellates and ciliates). The model can explain > 90% of the variation of a rich set of observations consisting of 11 independent variables over the course of 13 days during which a bloom largely dominated by diatoms develops, and disappears almost entirely. Fluxes estimated by the model point to the importance of coagulation (TEP formation) as a sink term for DOC, and a source term for POC. Consequently, aggregation with TEPs constitute an important loss term for phytoplankton. The flocculated phytoplankton, and detrital material, in turn become rapidly degraded by the particle attached bacteria and other protist heterotrophs. Through a scenario analysis, the relevance of nutrient-stress enhanced lysis rates; alterations between small and large DOC in phytoplankton exudates; and coagulation of smaller DOC molecules were investigated. Our results suggest that the former two processes have negligible effects in isolation, but when combined with the latter, they can synergistically cause substantial deviations in TEP formation, hence, in flocculation rates; and consequently in the peak magnitude of the diatom bloom, and in timing of its termination. Our results point to a need for better understanding of processes governing the termination of phytoplankton blooms, their inter-dependencies, and consequences on the global biogeochemical cycles.

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“…The current conceptualization of carbon fate following viral activity is termed the “viral shunt,” in which cell carbon is converted to both nonliving POC in the form of recalcitrant cellular components such as cell walls, and labile DOC in the form of nucleotides, amino acids, sugars, and lipids (Suttle 2007). Viral reprogramming of phytoplankton host cells can alter lipid composition (Rosenwasser et al 2014), nucleic acid synthesis rates (Rosenwasser et al 2014; Thamatrakoln et al 2019), and extracellular polysaccharide production (Nissimov et al 2018), as well as the pool of DOC released post‐lysis (Ma et al 2018; Zhao et al 2019; Kuhlisch et al 2021). A model by Jumars et al (1989) simulating labile DOC release from phytoplankton was revised by Wilhelm and Suttle (1999) to include viral lysis.…”

Section: The Sourcesmentioning

confidence: 99%

The Ocean's labile DOC supply chain

Moran

Ferrer‐González

et al. 2022

Limnology & Oceanography

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Microbes of the surface ocean release, consume, and exchange labile metabolites at time scales of minutes to days. The details of this important step in the global carbon cycle remain poorly resolved, largely due to the methodological challenges of studying a diverse pool of metabolites that are produced and consumed nearly simultaneously. In this perspective, a new compilation of published data builds on previous studies to obtain an updated estimate of the fraction of marine net primary production that passes through the labile dissolved organic carbon (DOC) pool. In agreement with previous studies, our data mining and modeling approaches hypothesize that about half of ocean net primary production is processed through the labile DOC pool. The fractional contributions from three major sources are estimated at 0.4 for living phytoplankton, 0.4 for dead and dying phytoplankton, and 0.2 for heterotrophic microbes and mesoplankton.

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Viral infection of algal blooms leaves a unique metabolic footprint on the dissolved organic matter in the ocean

Cited by 52 publications

References 64 publications

Changes in Microbiome Activity and Sporadic Viral Infection Help Explain Observed Variability in Microcosm Studies

Changes in Microbiome Activity and Sporadic Viral Infection Help Explain Observed Variability in Microcosm Studies

Growth, organic matter release, aggregation and recycling during a diatom bloom: A model-based analysis of a mesocosm experiment

The Ocean's labile DOC supply chain

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